Original Paper Audiology Neurotology Audiol Neurotol 2008;13:123–144 Received: January 3, 2007 DOI: 10.1159/000111784 Accepted after revision: July 27, 2007 Published online: November 30, 2007
Central Auditory Impairment in Unilateral Diencephalic and Telencephalic Lesions
a–c a, c d F r a n z i s k a B i e d e r m a n n Peggy Bungert Gerd Joachim Dörrscheidt a, b c D. Yves von Cramon Rudolf Rübsamen
a b Daycare Clinic of Cognitive Neurology, University of Leipzig, Max-Planck-Institute of Cognitive Neuroscience, and c Faculty for Biosciences, Pharmacy and Psychology, University of Leipzig, Leipzig , and d Department of General Zoology and Neurobiology, Ruhr University, Bochum , Germany
Key Words were able to master the interaural tests, which indicates the Psychoacoustic tests Cortical auditory processing preserved ability to lateralize sound sources to the left and Contralateral impairment Dichotic hearing to the right with either one of the auditory cortices left in- tact. Another 24 patients were studied who had lesions mostly close to but sparing the before-mentioned auditory A b s t r a c t structures. All of them showed unimpaired performance in The extent of perceptual impairment following unilateral le- all test alternatives. The results indicate the specificity of the sions in the auditory cortex, its thalamic or callosal afferents dichotic signal/noise tests for the identification of unilateral was studied with psychoacoustic tests. Thresholds for the lesions in thalamocortical auditory structures. In addition, discrimination of signal frequency, intensity and duration the results also point to the capacity of each telencephalic were acquired under three different conditions of head- hemisphere to process the full range of auditory lateraliza- phone stimulation (‘monaural’, ‘interaural’, and ‘dichotic sig- tion from left to right. Copyright © 2007 S. Karger AG, Basel nal/noise tests’) using the three-alternative forced-choice procedure. The different test alternatives generated distinct auditory percepts, which is in accordance with the assump- tion of specific signal processing at the level of the auditory Introduction brainstem and at thalamocortical auditory areas. Twenty- one patients from neurology were studied who suffered One striking difference between the functionality of from unilateral lesions in the auditory cortex, the auditory the central auditory system on the one hand and the vi- thalamus, or the acoustic radiation. Location and extent of sual or somatosensory systems on the other hand is in the the lesions were assessed by magnetic resonance imaging. extent of perceptual deficits following lesions of their cor- Monaural tests of either ear revealed no deficits in auditory tical representation sites. A lesion of the primary visual performance. The patients showed impaired discrimination of signal frequency, intensity and duration in the dichotic signal/noise tests, when the signals were presented to the Abbreviations: n = Noise signal presented ipsilesionally; n = ear contralateral and the noise ipsilateral to the lesion. With ipsi contra noise signal presented contralesionally; sipsi = pure-tone signal pre- inverted signal and noise stimulation, however, the thresh- sented ipsilesionally; s contra = pure-tone signal presented contrale- olds were in the range of age-matched controls. All patients sionally.
© 2007 S. Karger AG, Basel Rudolf Rübsamen 1420–3030/08/0132–0123$24.50/0 Fakultät für Biowissenschaften, Pharmazie und Psychologie, Universität Leipzig Fax +41 61 306 12 34 T a l s t r a s s e 3 3 E-Mail [email protected] Accessible online at: DE–04103 Leipzig (Germany) www.karger.com www.karger.com/aud Tel. +49 341 97 36723, Fax +49 341 97 36848, E-Mail [email protected] Downloaded by: Universität Leipzig 139.18.89.136 - 10/9/2013 11:18:50 AM cortex in one hemisphere will entail homonymous hemi- a comprehensive analysis of the system. This is because anopsia in the contralateral visual hemifield [Zeki, 1993; we are just at the beginning of the development of effec- Gray et al., 1997]. Likewise, unilateral injury of the pri- tive and reliable diagnostic tools for the assessment of mary somatosensory cortex will cause somatesthetic dis- central hearing impairments [Divenyi and Robinson, orders on the opposite side of the body [Woolsey et al., 1989; Griffiths et al., 2001; Bungert-Kahl et al., 2004]. So 1979; Bassetti et al., 1993; Adams et al., 1997]. A respec- far, most case reports hardly contain quantifiable data tive lesion of the auditory cortex in one hemisphere, how- that would enable a reliable evaluation of the severity and ever, has no such severe effects. Regardless of whether the specific quality of an auditory impairment across the dif- left or the right auditory cortex is affected, stimulation of ferent tests applied [Graham et al., 1980]. either of the two ears will still yield unimpaired detection A more detailed analysis of the distinctive features of thresholds [human: Jerger et al., 1969; Cranford et al., auditory processing in each of the two telencephalic 1982; Antonelli et al., 1987; cat: Cranford, 1979; review: hemispheres is currently hampered by the close linkage Cranford, 1984]. Due to multiple ipsi- and contralateral of the auditory system with the systems for speech per- convergence in the auditory brainstem [Moore and Osen, ception and speech production [Tervaniemi and Hug- 1979; Nieuwenhuys, 1984; Moore, 1987; Bazwinsky et al., dahl, 2003]. Particularly, the left-hemispheric dominance 2003], most fibers ascending from either auditory thala- of the language system complicates the assessment of au- mus to the respective ipsilateral auditory cortex convey ditory impairments associated with left-sided cortical in- binaural input [cat: Phillips and Irvine, 1983; Martin and juries. Tests that aim to evaluate the integrity of the audi- Webster, 1989; Reale and Brugge, 1990; Reser et al., 2000; tory system and make use of speech material as test sig- review: Imig et al., 1986]. In this respect, the auditory nals [Berlin et al., 1972; Musiek and Pinheiro, 1987; thalamocortical afferents differ from their respective vi- Eustache et al., 1990] rather than prephonemic signals sual and somatosensory counterparts, both of which pre- and/or require verbal responses from the subjects [Schul- dominantly convey contralateral information (i.e. visual hoff and Goodglass, 1969; Pinheiro, 1976; Musiek and hemifield projections in the visual system and unilateral Pinheiro, 1987; Musiek et al., 1990, 1994] cannot reliably somatotopic projection in the somatosensory system) verify whether a specific result is due to deficits in the [Basetti et al., 1993; Gray et al., 1997]. speech or in the central auditory system. Since the assess- In addition, the primary and secondary auditory areas ment of auditory processing in the left hemisphere is still of both cerebral hemispheres show strong reciprocal in- somewhat tentative [Zatorre et al., 2002a, b], also any terconnections [rodents: Budinger et al., 2000; cat: Imig comparative evaluation of specific impacts of left- or et al., 1986; Rouiller et al., 1991; nonhuman primates: right-hemispheric auditory lesions on auditory perfor- Fitzpatrick and Imig, 1980; Luethke et al., 1989; Pandya mance must remain questionable. Particularly in dealing and Rosene, 1993; Kaas and Hackett, 2000], which for the with aphasic patients, it is indispensable to differentiate primary visual cortex has only been described for projec- between deficits which are directly linked to the aphasic tion related to the visual midline [Segraves and Rosen- syndrome and auditory-perceptual deficits [Warren and quist, 1982; Aboitiz, 1992; Zeki, 1993] and is also less pro- Gardner, 1995; Scott and Johnsrude, 2003]. nounced in the somatosensory cortex [Karol and Pandya, To overcome these difficulties, we developed a com- 1971; Jones et al., 1979]. The existence of such connec- prehensive battery of psychoacoustic headphone tests tions provides evidence for a strong interhemispheric co- based on our knowledge of monaural and binaural-inte- operation in acoustic feature extraction as a special qual- grative processing at different levels of the central audi- ity of auditory processing. tory system [review: Irvine, 1992]. This test battery was While these facts challenge a detailed analysis of the specifically designed for the use in patients with acquired cortical auditory representation, they hamper the evalu- brain lesions [Bungert-Kahl et al., 2004]. All tests have ation of specific features of auditory processing in either low demands on the comprehension of instructions, and of the two hemispheres. To date, the dissociation between they do not require verbal statements of the subjects. primary, secondary and tertiary auditory areas as well as Thus, they can be successfully employed even in aphasic the interhemispheric cooperation and the functional re- patients as well as in patients who suffer from various lation between auditory areas and neighboring sensory forms of cognitive deficits. The test battery comprises speech areas is far from being understood. three different subtests which all measure the discrimi- So far, data from patients suffering from focal lesions nation thresholds for the basic acoustic features frequen- in the respective cortical areas have contributed little to cy, intensity, and signal duration. The first subtest is
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Downloaded by: Universität Leipzig 139.18.89.136 - 10/9/2013 11:18:50 AM T a b l e 1 . Test parameter overview
Test Test Frequency of test signals, kHz Signal Ramp Intensity Initial Mode of tests Initial Final variable duration ms value step step ms size size
Audiogram SPL 0.125/0.25/0.5/1.0/2.0/4.0/8.0/16.0 250 10 – 60 dB SPL additive 10 dB 2 dB Frequency discrimination F, Hz 0.25/0.5/1.0/2.0/4.0/8.0 250 10 30 dB SL 1000 Hz multiplicative 2.0 1.1 Intensity discrimination I, dB 0.5/1.0/2.0/4.0 250 10 30 dB SL 20 dB additive 5 dB 2 dB Duration discrimination D, ms 0.5/1.0/2.0/4.0 250 10 30 dB SL 100 ms additive 10 ms 3 ms Phase discrimination , ° 0.25/0.5/1.0 500 20 30 dB SL 140° additive 15° 7°
based on monaural (monotic) signal presentation, the Materials and Methods second uses binaural stimulations with interaural differ- ences of the respective acoustic features in any case caus- Stimuli and Test Procedure The psychoacoustic test procedures were automatized using a ing lateralized auditory percepts. The third subtest em- psychoacoustic setup (Tucker-Davis Technologies, TDT, System ploys the dichotic presentation of signal/noise (s/n) pairs, II) and associated software (SigGen, PsychoSig). Measurements a test paradigm already used by Thompson and Abel were performed in a sound-attenuated booth (Industrial Acous- [1992]. Here, the subjects receive test signals through one tics). In each patient, we first acquired the audiogram and the ear and concurrently bandpass-noise bursts through the detection thresholds for bandpass noise [0.1–20 kHz; yes/no (heard/not heard) paradigm]. Thereafter, the discrimination other ear. This test design aims to evaluate cortical audi- thresholds for specific acoustic features were assessed using three tory processing by quantifying the degree of central test alternatives (see below for a detailed description) and an masking of the test signals through the noise signals adaptive one-up one-down method, measuring the 50% correct [Zwislocki, 1972; Mills et al., 1996]. These three modes of point of the psychometric curve [P(x) = 0.5] [Levitt, 1970]. stimulation are associated with different types of audi- In all tests, stimuli were presented through headphones (Bay- er-Dynamic 770-Pro) at 30–35 dB SL (sensation level), i.e. at con- tory percepts and (in part) linked to differences in audi- stant above-threshold levels in each subject. This level guaranteed tory performance which can be used to define irregular- a moderate loudness of the stimuli, but excluded any crosstalk ities or a potential breakdown in central processing at from one headphone transducer to the contralateral ear, which various levels of the ascending auditory system. An ad- could have obscured the results. Stimulus duration was 250 ms ditional advantage is the independence from the func- including 10 ms cosine-square ramps; interstimulus interval was 750 ms. tioning speech system, which allows for an immediate Tests were designed to scrutinize the just noticeable differ- comparison of auditory processing in both cortical hemi- ences for tone bursts differing in the basic acoustic features fre- spheres. quency, intensity or duration (table 1 summarizes the signal pa- The present investigation focuses on patients who suf- rameters applied). Three different test alternatives were used: (1) fered from unilateral lesions in diencephalic and/or tel- monaural tests, i.e. monaural signal presentation to either ear, (2) dichotic s/n tests, i.e. dichotic presentation of s/n pairs, and (3) encephalic auditory structures which included the me- interaural tests, i.e. binaural signal presentation with interaural dial geniculate nucleus, the acoustic radiation and/or the signal differences (see below for an evaluation of the percepts re- transcallosal fibers interconnecting the auditory corti- lated to the different stimulus modes). ces, or the auditory cortex itself. The results show that The three-alternative forced-choice method was used in all dichotic s/n tests are sensitive and at the same time robust discrimination tests. Subjects were asked to differentiate between reference signals and test signals differing in a single acoustic fea- diagnostic tools that help to identify hemispheric-specif- ture with the position of the test signal randomly altered within ic impairments of auditory processing. Detailed descrip- the stimulus triplet. Such tests are manageable even without the tions of distinct auditory impairments are given here for subjects being aware of the specific acoustic property that was selected patients for whom the precise localization of the varied during testing. As long as the subjects were able to apply brain lesions is known from MRI. The correspondence the concept of ‘same’ and ‘different’ to three successively present- ed acoustic signals, and to indicate, with some consistency, the between specific deficits in auditory processing and spe- one detected as different, the tests yielded a reliable outcome. cific patterns of brain lesions suggests such tests as psy- Such a standardized test design was chosen to minimize the chophysical tools for the immediate diagnosis of the re- amount of instructions necessary to explain every single test to spective dysfunction. the subjects. Preliminary evaluation of the tests in a variety of patients from the Daycare Clinic of Cognitive Neurology dis- closed the strength of this procedure, which enabled reliable eval-
Hemispheric-Specific Auditory Audiol Neurotol 2008;13:123–144 125 Impairment Downloaded by: Universität Leipzig 139.18.89.136 - 10/9/2013 11:18:50 AM T a b l e 2 . Lesions and etiology of all cases included in this study
Pa- Age Etiology Pa- Age Etiology tient tient
Patients with psychoacoustic deficits Control patients Lesion in the right auditory cortex Patients with infarction of the posterior cerebral artery 148 46 Ruptured aneurysm of the middle cerebral artery, 246 71 Cerebral microangiopathy and macroangiopathy: vasospastic stroke of middle cerebral artery infarction of the posterior cerebral artery bilateral 178 38 Aneurysm of the atrial septum, cardiac-embolic 298 45 Cerebral microangiopathy and macroangiopathy: stroke of the middle cerebral artery infarction of the posterior cerebral artery left, 566 44 Hemorrhagic stroke of the middle cerebral artery infarction of the cerebellum left 640 57 Stroke of the middle cerebral artery 431 37 Stroke of the posterior cerebral artery left 649 19 Stroke of the middle cerebral artery 454 66 Stroke of the posterior cerebral artery left 465 47 Cerebral microangiopathy and macroangiopathy: Lesion in the left auditory cortex infarction of the posterior cerebral artery right 085 42 Stroke of the middle cerebral artery 484 48 Infarction of the cerebellum left 341 6 7 Stroke of the middle cerebral artery stroke of the posterior cerebral artery right 448 6 9 Hemorrhagic stroke of the middle cerebral artery 496 5 2 Intracerebral hemorrhage, 537 4 0 Cerebral micro- and macroangiopathy: stroke of stroke of the posterior cerebral artery right the middle cerebral artery 516 3 3 Stroke of the posterior cerebral artery left 574 5 2 Intracerebral hemorrhage of putamen-claustrum 547 7 3 Cerebral microangiopathy and macroangiopathy: type, cerebral microangiopathy stroke of the posterior cerebral artery left 577 6 1 Stroke of the middle cerebral artery 559 7 2 Cerebral microangiopathy and macroangiopathy: 619 5 2 Stroke of the middle cerebral artery stroke of the posterior cerebral artery right 662 60 Stroke of the middle cerebral artery 593 5 6 Stroke of the posterior cerebral artery right 625 68 Cerebral microangiopathy and macroangiopathy: Lesion of subcortical auditory structures stroke of the posterior cerebral artery bilateral 046 59 Posterior cortical watershed infarction, 667 34 Stroke of the middle cerebral artery left and cerebral atherosclerotic microangiopathy posterior cerebral artery left 130 48 Mycotic aneurysm 750 61 Stroke of the middle cerebral artery left and 214 47 Cerebral microangiopathy: intracerebral posterior cerebral artery right hemorrhage of putamen-claustrum type (progressive form) Lesion of the temporal pole 228 59 Cerebral microangiopathy 236 26 Head injury, transient global ischemia 289 4 1 Hemorrhage of the thalamus 252 48 Astrocytoma/lobectomy left 305 6 3 Atherosclerotic vessels, cerebral microangiopathy 372 28 Venous infarction left and macroangiopathy 761 40 Tumor/resection right, suspected brain stem 327 5 5 Stroke of the middle cerebral artery infarction 522 48 Intracerebral hemorrhage Lesion of the basal ganglia and of the internal capsule 302 68 Microangiopathy: ischemic infarction of the poste- rior branches of the lateral striolenticular arteries 353 43 Intracerebral hemorrhage 435 69 Cardiac-embolic hemorrhagic stroke of the middle cerebral artery, cerebral microangiopathy 479 55 Cerebral microangiopathy 496 52 Intracerebral hemorrhage, stroke of the posterior cerebral artery right 750 61 Stroke of the middle cerebral artery left, stroke of the posterior cerebral artery right
uation of auditory perception even in patients suffering from re- What makes these tests suitable for the evaluation of central duced comprehension of instructions [see also Bungert-Kahl et auditory processing capacity? In all test alternatives the subjects al., 2004 for more details on the test procedures and for the dis- have to compare internalized percepts associated with three crimination thresholds for the respective tests in normal-hearing acoustic events after the whole of the stimulus triplet has been naive subjects aged 20–70 years]. presented.
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Downloaded by: Universität Leipzig 139.18.89.136 - 10/9/2013 11:18:50 AM (1) In the monaural tests these percepts convey deviant infor- S u b j e c t s mation about a single acoustic feature, frequency, intensity, or sig- The data included in this report were collected from 45 patients nal duration. The discrimination limens for the respective fea- selected from a sample of more than 1000 patients of the Daycare tures indicate the capacity of central processing (which self-evi- Clinic of Cognitive Neurology of the University of Leipzig, all suf- dently is also limited by the constraints of middle ear signal fering from acquired brain lesions. Patients were only included in transmission and cochlear signal transduction). the study (i) if they suffered from a physiological inner ear hearing (2) The dichotic s/n tests were – with regard to the test system- loss of less than 20 dB, (ii) their brain lesions showed clear demar- atics – an extension of the monaural tests, as here the signal pre- cations which included central auditory structures (hearing-im- sentation to one ear was paired with bandpass noise bursts (0.1–20 paired patients) or (iii) were close to but spared auditory structures kHz; 250 ms) presented to the other ear. The noise is intended to (control patients). In performing the tests, the cognitive status of interfere with processing of the test signals, causing central audi- the patients was taken into consideration, e.g. in patients suffering tory masking [Zwislocki, 1972; Mills et al., 1996]. from aphasia extra efforts were made when necessary in order to (3) In all interaural tests, the presentation of identical signals ensure that the test instructions were understood to guarantee the to the two ears constituted the reference condition (dichotic stim- reliability of our data on central auditory discrimination. All sub- ulation). For acquisition of interaural frequency difference limens jects participated on a voluntary basis and gave written informed (DL) the test variable was frequency at the two ears (both start- consent. The study was approved by the ethics committee of the ing at cosine), for interaural intensity differences the test variable University of Leipzig and conforms with The Code of Ethics of the was intensity, and for interaural duration difference signal du- World Medical Association (Declaration of Helsinki). The diagno- ration. The interaural test alternative additionally allows testing sis of the specific quality, the location, and the size of the brain for phase differences ( phase) in tone bursts presented with the damage was based on neurological examinations and on neuroim- same frequency ( ! 1 kHz) at both ears. Common to all these in- aging data (CT; MRT: 3T, three -dimensional analysis). In addition, teraural mismatches is the induction of sound percepts that ap- but not directly related to the psychoacoustical evaluation of audi- pear intracranially lateralized on an interaural axis as compared tory perception, all patients received extensive neurological, neu- to on-center percepts connected to the reference stimuli. Lateral- ropsychological, and speech therapy at the Daycare Clinic. The ization appears static for intensity and phase and ‘moving’ for patients studied will be introduced according to the location of frequency and signal duration. Interestingly, the naive subject their brain tissue damage (table 2 ). is not able to identify which acoustic feature is varied in any of the interaural tests (see ‘Results’ for a more detailed evaluation of the Patients with Cortical Lesions percepts related to the different stimulus modes). Five patients (patients 178, 148, 566, 640 and 649; age 19–57 The fact that the monaural and the dichotic s/n tests on the years, mean age 40.8 years) suffered from extended lesions in the one hand and the binaural tests on the other hand generate fun- superior temporal gyrus of the right hemisphere which included damentally different percepts points to different neural substrates the entire Heschl’s gyrus comprising the primary auditory cortex involved in the respective signal processing. This assumption is and parts of auditory association areas. substantiated by significant differences in the threshold values Concerning damage of the left hemisphere, 8 patients (pa- between the two test modes. tients 085, 341, 448, 537, 574, 577, 619, and 662; age 40–69 years, Each patient was studied in two to four 45-min morning ses- mean age 55.1 years) were studied, who had lesions of different sions. The patients performed in eleven different psychoacoustic etiology in the left auditory cortex, which in some cases extended discrimination tests each applied considering the individual de- to the associated subcortical white matter and to the insula. tection thresholds separately evaluated for each ear. During the tests, the subjects communicated their stimulus selections through Patients with Subcortical Lesions a response box equipped with three push-buttons and three LEDs. In another 8 male patients, age 43–69 years (mean age 53.2 Those patients who, because of motor and/or cognitive deficits, years), left-sided subcortical lesions of different etiology were di- were incapable of handling the response box responded directly agnosed in the area of the basal ganglia and the posterior inferior to the tester by other means of communication (e.g. by pointing thalamus (including the medial geniculate nucleus). In the pa- to colored circles). During each test, no time limits were set for the tients 046, 130, 214, 228, 289, 305, 327 and 522 these lesions led to subjects’ selection of the deviant signal in the triplet. If the sub- a deafferentation of the left auditory cortex, which itself was left jects expressed an uncertainty about the position of the deviant intact ( table 2 ). signal, they were encouraged to make guesses. The results ob- tained in the different tests can be regarded as independent vari- C o n t r o l P a t i e n t s ables, since each test was performed at different frequencies. El- Three groups of patients characterized by lesions in the vicin- evated threshold values were checked by test repetitions. The test ity of cortical and subcortical auditory structures, but leaving supervisor was not informed about the exact localization of the those structures unaffected, served as controls. Fourteen patients brain lesions in the patients. (age 33–73 years; mean age 51.5 years) had lesions caudal to The evaluation of impaired perception of specific acoustic Heschl’s gyrus due to infarctions of the posterior cerebral artery cues in the patients was based on the comparison of the perfor- of the right or left hemisphere. The lesions typically included the mance with that of age-matched naive, normal-hearing subjects occipital lobe and in many cases also basal and/or caudal aspects [Bungert-Kahl et al., 2004]. The data were quantified by calculat- of the temporal lobe. ing z scores. Four patients (age 26–48; mean age 35.5 years) had lesions in the rostral pole of the temporal lobe (3 left, 1 right). In all of these cas- es Heschl’s gyrus and its immediate vicinity were not affected.
Hemispheric-Specific Auditory Audiol Neurotol 2008;13:123–144 127 Impairment Downloaded by: Universität Leipzig 139.18.89.136 - 10/9/2013 11:18:50 AM Six patients (age 43–69; mean age 58.0 years) served as subcor- tical controls. All of them had lesions in the basal ganglia and in the region of the internal capsule of the left hemisphere. Included in this group were cases in which the medial geniculate nucleus, the acoustic radiation and presumably also interhemispheric au- ditory connections were left intact.
R e s u l t s
Patients with Impaired Auditory Discrimination
Right Auditory Cortex Lesion Impaired discrimination of acoustic features linked to F i g . 1 . MRT images, patient 178, lesion in the right superior tem- an extended lesion in the area of the right auditory cortex poral plane, transversal (A ) and coronal view ( B ). The arrows will be exemplified in detail for patient 178. In this 38- point to the intact Heschl’s gyrus on the left superior temporal plane. For details on lesion and etiology see table 2. year-old woman, an infarction of the right middle cere- bral artery had caused a pseudocystically transformed necrosis which included – among other structures – the right superior temporal gyrus (fig. 1, table 2). The patient For the same patient also the just noticeable intensity was tested 22 months after the insult. discrimination was in the range of age-matched controls, Pure-tone audiometric examination showed for both both if either the left or the right ear was stimulated mon- ears a 5- to 10-dB elevation of thresholds for frequencies aurally ( fig. 2 D). In the dichotic s/n tests, as in the respec- up to 1 kHz and mostly normal thresholds for higher fre- tive tests for frequency discrimination, an ipsilesional quencies ( fig. 2 A). presentation of level differences gave normal results, Difference limens for monaural frequency discrimi- while the presentation of test signals contralateral to the nation tested at 30–35 dB SL for each frequency was (with lesioned side resulted in strongly elevated intensity dif- one exception) in the range of age-matched normal-hear- ference limens ( fig. 2 E). ing subjects, irrespective of whether the test signals were The results for the discrimination of tone duration dif- presented ipsilaterally (right ear) or contralaterally (left ferences shared the same characteristic pattern as found ear) to the lesioned auditory cortex (fig. 2B). Unimpaired in the above-mentioned tests (fig. 2F, G). Signal discrim- frequency discrimination was for the most part also seen ination in the monaural tests was mostly in the range of in dichotic s/n tests with test signals presented ipsilater- age-matched normal controls. In the dichotic s/n tests, ally to the lesion (fig. 2 C). If, however, the test signals ipsilesional presentation of the test signals again gave in- were presented contralaterally and the noise ipsilaterally conspicuous results, while the contralesional presenta- to the lesioned cortex, frequency discrimination was sig- tion of the signals yielded significantly poorer perfor- nificantly reduced. mance at all three test frequencies employed.
F i g . 2 . Auditory performance of patient 178 compared with age- Intensity discrimination limens for monaural ipsilesional (right) matched normal-hearing subjects. Audiograms for both ears and contralesional (left) stimulation ( D) vs. dichotic sipsi /n contra show slightly elevated thresholds for low and middle frequencies, and dichotic s contra /nipsi stimulation ( E ) (symbols as in B, C). For but mostly normal detection thresholds for frequencies 1 2 kHz intensity discrimination the normative data give no indication of (A ). Mean detection thresholds ( 8 SD) for normal-hearing 30- to a systematic change with stimulus frequency. Discrimination li- 39-year-old subjects are shown by solid black line [normative data mens for signal duration tested with monaural (F ) and with dich- by Bungert-Kahl et al., 2004]. The just noticeable (jn) frequency otic s/n stimulation (G ) (symbols as in B , C). Note that for almost difference limens for monaural ipsilesional (right _ ) and contra- all monaural tests the results of patient 178 ( B , D, F ) were in the lesional (left +) stimulation ( B) vs. dichotic sipsi /n contra (y ) and normal range of age-matched controls, as were the results for the dichotic s contra /nipsi (I ) stimulation (C ). Mean discrimination dichotic tests with the signals presented to the ipsilesional ear thresholds ( 8 SD) for normal-hearing 30- to 39-year-old subjects (open symbols in C , E , G ). Elevated thresholds in the dichotic dis- are shown by solid black line. For frequency discrimination the crimination tasks were consistently found when the test signals difference limens typically worsen with increasing test frequency. were presented contralaterally to the lesioned cortex.
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Downloaded by: Universität Leipzig 139.18.89.136 - 10/9/2013 11:18:50 AM Audiogram 100 30–39 years 90 178 right 80 178 left 70 60 50 40 30 20 10
Hearing threshold (dB SPL) Hearing threshold 0 –10 0.125 0.25 0.5 124816 A Frequency (kHz) Monaural Dichotic s/n 30–39 years 30–39 years 178 right 100.0 178 right 100.0 178 left 50.0 178 left 50.0
10.0 10.0 5.0 5.0
1.0 1.0 0.5 0.5 jn frequency difference (Hz) jn frequency difference Frequency (Hz) jn frequency difference Frequency
0.25 0.50 1.00 2.00 4.00 0.25 0.50 1.00 2.00 4.00 BCFrequency (kHz) Frequency (kHz)
18 18 Intensity Intensity 16 16 14 14 12 12 10 10 8 8 6 6 4 4
jn intensity difference (dB) jn intensity difference 2 (dB) jn intensity difference 2 0 0 0.5 1.0 2.0 4.0 0.5 1.0 2.0 4.0 DEFrequency (kHz) Frequency (kHz)
200 200 Duration Duration 180 180 160 160 140 140 120 120 100 100 80 80 60 60 40 40
jn duration difference (ms) jn duration difference 20 (ms) jn duration difference 20 0 0 0.5 1.0 2.0 4.0 0.5 1.0 2.0 4.0 FGFrequency (kHz) Frequency (kHz) 2
Hemispheric-Specific Auditory Audiol Neurotol 2008;13:123–144 129 Impairment Downloaded by: Universität Leipzig 139.18.89.136 - 10/9/2013 11:18:50 AM Auditory Patient 178 Diencephalic and telencephalic auditory processing brainstem
Interaural f Monaural f Dichotics/n f Frequency 0/0/0 0/0/– 0/2/0 0/0/011/4/20 0/2/0
Interaural I Monaural I Dichotics/n I Intensity 0/1/–/– 0/–/0/– 0/0/–/– 0/0/–/–11/16/6 0/0/0/–
Interaural t Monaural t Dichotics/n t
0/0/–/– 1/–/–
Duration/IPD IPD 0/0/2/0 0/0/0/0 13/19/15 0/0/0/–
–/0/– 1/–/–
Ear/percept Left side Right side Left ear Right ear Left ear Right ear
F i g . 3 . Psychoacoustic data sheet for patient 178, a 38-year-old cies: 0.25/0.5/1.0 kHz). The results from the different test alterna- woman who was tested 22 months after the insult. All values are tives (interaural, monaural, dichotic s/n ) are shown from left to z scores for different test frequencies indicating the deviation of right, pointing to signal processing at different levels of the central the respective measurement from the mean values in 30- to 39- auditory system. Auditory brainstem: the interaural tests assess year-old normal-hearing subjects as multiples of SD (fig. 2). As the thresholds for the generation of a lateralized percept by a re- indicated in the bottom-most row, the different columns show the spective interaural feature difference. Diencephalic and telence- performance related to the signal presentation to the left or the phalic auditory processing: results of the monaural and dichotic right ear, respectively, lateralized percept to the left or to the right s/n tests are shown with respect to signal presentations to the left side. The different rows show (from top to bottom) the frequency or the right ear. In the dichotic s/n stimulation, the noise was pre- discrimination limens ( f, test frequencies: 0.25/0.5/1.0 kHz), in- sented to the other ear. Note that consistently elevated z scores tensity discrimination limens ( I, test frequencies: 0.5/1.0/2.0/4.0 were only found under the condition of dichotic s/n stimulation, kHz; [–] indicates missing data points), duration discrimination and only if the signals were presented contralaterally to the le- limens ( t, test frequencies: 0.5/1.0/2.0/4.0 kHz), and (only for in- sioned cortex. teraural tests) the phase discrimination limens (IPD, test frequen-
The patient was able to master the interaural tests frequency, intensity, and signal duration. In order to pres- based on the presentation of frequency, intensity, phase, ent the data in a form which enables an immediate com- and signal duration differences at the two ears generating parison between different test results within and between intracranially lateralized (stationary or moving) per- subjects and also allows an evaluation of the severity of a cepts. Discrimination thresholds were in the range of respective impairment, z scores were calculated relating age-matched controls for lateralization to the left and to single measurements to the standard deviation of norma- the right side [for respective reference values see Bungert- tive data (fig. 3). These nondimensional quantifiers ad- Kahl et al., 2004]. ditionally have the advantage of promoting the compari- It must be emphasized that a contralesional signal pre- son of test results that differ on a large numeric scale (e.g. sentation paired with noise bursts delivered to the other intensity and frequency difference limens). ear (dichotic s/n stimulation) was the only stimulus con- The synopsis presented in figure 3 shows the frequen- dition which consistently yielded the impaired discrimi- cy-specific z scores for signal presentation to the respec- nation threshold for all three acoustic features tested, i.e., tive ear in the monaural and dichotic s/n tests and for left
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Downloaded by: Universität Leipzig 139.18.89.136 - 10/9/2013 11:18:50 AM T a b l e 3 . Summary of the performance of the subjects in the different tests
Pa- Age Sex MPI CPP Frequency difference limens Intensity difference limens Duration difference limens tient interaural monaural dichotic s/n interaural monaural dichotic s/n interaural monaural dichotic s/n
S i S c Si Sc Si /N c Sc /N i Si Sc S i S c Si /Nc Sc /Ni Si Sc Si Sc S i/N c S c/N i
Auditory cortex right hemisphere 148 46 F 18 + 1 1 0 0.3 0.5 11 0.3 0.5 0 0 0 2.5 0 0 0 0 0 4.2 178 39 F 22 – 0 0 0 0.6 0.6 11.6 0 0.5 0 0 0.3 11 0 0 0 0.5 0 15.6 566 44 M 9 + 0 0 1 0 0.4 8.8 – – 0.5 0.5 0.6 13 0.1 6.3 11 1 1 640 57 M 20 – 0 2 0 0 0 1.6 0 2 0 0 0.5 6 0.5 4.5 0 0.5 0 5 649 67 M 19 – 0 10.5 00016.3 0 0.3 0 0 0.5 7 0.3 1.5 0 0.6 0 2.6
Auditory cortex left hemisphere 085 42 M 36 – 0 0.3 0 0.2 0 8.6 0 1.6 0 0 0 5.3 0 0 0 0 0 4.7 619 52 M 30 + 0 0 1 0.5 0.5 20 – – 0 0.3 0.6 9.3 0 1 0 0.5 0 8.7 341 63 M 2 + 0 0 0 0 0.2 2 0 0.3 0 2 1.3 4.6 20 20 1.2 3 3 4.7 448 69 M 2 ? 0 1.3 0.6 0 0.3 11.6 0 1.6 0.6 0 0.6 11.3 0 0 2 4 4.5 12 537 40 F 11 ? 0 0 1.5 0 0 2.6 – – 0 0 0.6 10.3 1 1 3.5 1.5 8.5 18 574 52 M 5 – 0 0 0 0 0.2 6 0 0 0 0.2 0 6.7 0 0 5 2.5 9 11.5 57761M4–0 0001 20 0.300.600 5 10 4 4.6 3.6 5.5 662 62 M 1 – 0.3 0 0 0.6 0 17 0 0.5 0.5 0 0 10.3 8 10 7.5 5.5 6.5 14 Unilateral deafferentation of auditory cortex left hemisphere 046 59 M 71 + 0 0 0 0.3 0 8.6 0 0 0 0 0 8 0 0.5 0 0 0 1.6 214 48 M 24 + 0 0 0 0 0 3.6 0 1.7 0.3 0.3 0 15.5 1 0.3 0.6 1 0.2 14 228 59 M 4 + – – 0 0 – – – – 0 0 0 5 – – 0 1 0 2 305 62 M 2 – 0 0.3 0 0 1.6 5 0 0 1 0.2 0.7 6.2 0.5 0 0 0 0.2 3.7 327 55 M 5 + 0 2.6 0 0.6 0.6 6.3 0 1.6 0 0 0.3 7.6 0.5 0.5 1.7 4 3 9.5 522 48 M 14 – 0 0 1 0 0 1.2 – – 0 0 0.5 3.3 0.5 0 4.5 3 6 3 130 48 M 42 + 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 289 41 M 1 – 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
The table is arranged according to the site of lesions. Indicated are the Nc = noise bursts presented ipsilesionally or contralesionally, respectively. patients’ ID, sex, post-insult months (MPI), and whether (+) or not (–) the Numbers indicate mean z scores for all tested frequencies in the respective patient showed signs of the ‘cocktail party phenomenon’ (CPP), i.e. indica- tests. See the ‘Results’ section for a closer description of the types of corti- tion of deficits in speech comprehension in noisy environment. Si and Sc = cal lesions and the respective auditory performance. Tone pulses presented ipsilaterally or contralaterally, respectively; Ni and
and right lateralization in the interaural tests. The three Four other patients (148, 566, 640 and 649) with compa- noticeable findings were (i) good execution of the mon- rable lesions of the right temporal lobe gave equivalent aural tests for stimulation of either ear, (ii) preserved abil- results in the monaural, interaural and dichotic s/n tests ity to lateralize sound signals on the basis of interaural (table 3). In some of these patients, the interaural tests signal differences, and (iii) distinct differences in the generating auditory percepts lateralized to the contrale- dichotic s/n tests in which the performance worsened as sional side also yielded elevated thresholds, but this was soon as the test signals were presented contralaterally to most likely due to a multimodal neglect that these pa- the lesioned auditory cortex. Analysis using t test revealed tients also suffered from. significant deviations from age-matched normative val- ues for all acoustic cues and all tested frequencies in the Left Auditory Cortex Lesion dichotic s/n tests when the signals were presented contra- The 8 patients included in the present study with le- laterally, but not when they were presented ipsilaterally to sions in the superior temporal gyrus of the left hemi- the lesioned auditory cortex (contralesional signal: p ! sphere (patients 085, 341, 448, 537, 574, 577, 619 and 662) 0.001 for the discrimination of frequency, intensity, and mostly showed corresponding, mirror-inverted patterns tone duration differences). of impairment ( table 3 ). Patients 341, 448, 537, 574, 577 The data shown here for patient 178 represent a typical and 662 additionally suffered from elevated thresholds example for the performance in psychoacoustic tests fol- for duration discrimination observed under monaural lowing a right-hemispheric lesion of the auditory cortex. test conditions as well as in the dichotic s/n tests with an
Hemispheric-Specific Auditory Audiol Neurotol 2008;13:123–144 131 Impairment Downloaded by: Universität Leipzig 139.18.89.136 - 10/9/2013 11:18:50 AM Auditory Patient 448 Discrimination of basal acoustic parameters brainstem
Interaural f Monaural f Dichotics/n f Frequency 0/0/– 4/0/0 2/0/0 0/0/0 1/0/0 4/11/20
Interaural I Monaural I Dichotics/n I Intensity 0/0/0/– 0/2/3/– 0/2/0/– 0/0/0/– 2/0/0/– 13/11/10
Interaural t Monaural t Dichotics/n t Duration 0/0/–/– 0/0/–/– 1/3/–/– 4/4/–/– 5/4/–/– 15/10/11
Ear/percept Left side Right side Left ear Right ear Left ear Right ear
F i g . 4 . Psychoacoustic data sheet for patient 448. All values are z crimination of duration differences is indicated by elevated scores indicating the deviation of the actual measurement from thresholds in monaural and dichotic s/n tests of for both ears. Due the mean values in 60- to 69-year-old normal-hearing subjects as to reduced attention spans, patient 448 repeatedly produced ele- number of SD. Design of the graph as in figure 3. Note that im- vated thresholds in single runs of tests which he typically could paired discrimination for frequency and intensity differences was master. Note that as in patient 178 (fig. 3) consistently elevated z consistently found in the dichotic s/n tests with the signals pre- scores were mostly measured in dichotic s/n tests with the signals sented to the right ear. Additionally, a general impairment of dis- presented contralaterally to the lesioned cortex.
ipsilesional signal presentation. Patient 448 (69 years old), mal-hearing subjects. The contralesional signal presenta- e.g., was diagnosed with an extended lesion in the left tion in the dichotic s/n tests yielded even worse results Heschl’s gyrus due to a hemorrhagic infarction of the with tone duration discrimination possible only at differ- middle cerebral artery, which had led to an incomplete ences as large as 160–185 ms (z scores 10–15). Table 3 necrosis along the superior temporal gyrus (table 2). The summarizes the data from all patients with left auditory patient showed a distinct pancochlear hearing loss for cortex lesions (patients 341, 537, 574, 577 and 662) who both ears, which was taken into account in all discrimi- had auditory impairments comparable to those of patient nation tests by presenting the signals at 30–35 dB SL. 448. Stimulation of either ear in the monaural tests, stimula- The consistent pattern of test results in a subgroup of tions generating left- or right-lateralized signals in the patients with left-hemispheric lesions might indicate a interaural tests, and ipsilesional signal presentation in the superposition of two distinct modes of impairments: (i) a dichotic s/n tests yielded mostly normal difference li- reduced capacity for the discrimination of all tested mens for intensity and frequency discrimination. Elevat- acoustic features revealed in the dichotic s/n tests with ed discrimination thresholds were found in dichotic s/n contralesional (right) signal presentation, and (ii) a more tests with the signals presented to the ear contralateral to extensive deficit for tone-duration discrimination which the lesion. In this respect, the results are directly compa- appears to be independent of the test modes and of the rable to those associated with lesions of the right auditory stimulated ear. cortex. What differed, however, were the results from du- The differences found in the patterns of impairment ration discrimination tests. Here, already the monaural after lesions of the left or the right auditory cortex areas stimulation of either ear, as well as the ipsilesional signal might point to differences in auditory processing in the presentation in the dichotic s/n tests, yielded moderately two cortical hemispheres. At least lesions in the superior elevated difference limens ranging up to 70–85 ms (z temporal gyrus of the non-speech-dominant hemisphere scores 1–5; fig. 4) compared to about 20 ms found in nor- never led to impaired discrimination of tone duration
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Downloaded by: Universität Leipzig 139.18.89.136 - 10/9/2013 11:18:50 AM differences. Alternatively, the differences in the results following left and right auditory cortex lesions might re- flect slight differences in the extent of lesioned areas in the left and right hemisphere. The present data do not al- low us to rule out either of the two possibilities. This issue requires an additional in-depth analysis, which will be the subject of a prospective study.
Unilateral Deafferentation of the Auditory Cortex In the patients discussed above, the lesions had direct- ly affected the auditory cortex. Additionally a group of patients was studied, in which magnetic resonance to- mography (MRT) showed that Heschl’s gyrus itself had remained intact, but was found to be deprived of its tha- F i g . 5 . MRT image, patient 305, horizontal (A ) and coronal view lamic afferents and of its auditory input from the contra- ( B ). Subcortical lesions (white arrows) were found in the posterior lateral auditory cortex conveyed through the corpus cal- thalamus and the pars retrolenticularis affecting the left medial geniculate nucleus and interrupting the acoustic radiation and losum. The impairments in auditory discrimination as- most likely also associated transcallosal auditory fibers. sociated with such pathologies will be described for patient 305 ( table 2). This 63-year-old man suffered from an infarction which – on the left side – had caused a ne- crosis of the posteroinferior thalamus including the me- still yielded elevated difference limens in all dichotic s/n dial geniculate nucleus and the adjacent proximal por- tests (fig. 7). Compared to the data of age-matched con- tion of the acoustic radiation (fig. 5). trols, the differences were highly significant (p ! 0.001 for Pure-tone audiometric examination in this patient all tested frequencies). showed normal thresholds for both ears at low and mid- Three more patients (046, 214 and 228, table 2) with dle frequencies but a noticeable bilateral sensorineural left-hemispheric subcortical lesions affecting large por- hearing loss at frequencies 1 2 kHz ( fig. 6 A), which was tions of the acoustic radiation and thus deafferenting compensated for in the discrimination tests. The perfor- Heschl’s gyrus were subjected to the same test battery. In mance in all monaural auditory tests was mostly in the all 3 of them, the psychoacoustic measurements showed normal range of age-matched controls (fig. 6B, D, F). The the same characteristic profile of impairment as de- interaural tests, evaluating the ability of the patient to scribed for patient 305 (table 3). The profile of the psycho- lateralize sound sources based on differences in single acoustic data of patients 327 and 522 additionally showed acoustic features, yielded inconspicuous results as well impaired discrimination of tone duration in monaural (fig. 7). Occasionally elevated thresholds occurred, which tests of either ear, a pattern that was repeatedly seen after did not show any systematic dependency with respect to left Heschl’s gyrus lesions (e.g. patient 448). the stimulated ear or the acoustic parameters. It is un- All patients reported above showed rather consistent likely that these sporadic threshold elevations point to a patterns of impairment in the psychoacoustic tests. All specific central auditory impairment. They may rather be cases diagnosed with a right-hemispheric and 2 cases attributed to attention deficits (typically causing such un- with a left-hemispheric lesion of the auditory cortex (pa- stable performance) possibly linked to the marked micro- tients 085 and 619), as well as a number of those diag- angiopathic changes observed in the MRT images. nosed with an interruption to the left acoustic radiation In the present case, like in patient 178 described above, (patients 046, 214, 228 and 305) showed elevated differ- the discrimination of tone frequency, intensity, and dura- ence limens in dichotic s/n tests for frequency, intensity tion was mostly unimpaired in the respective dichotic s/n and duration discrimination when the signals were pre- tests when the test signals were presented ipsilaterally to sented to the contralesional ear (fig. 8A; n = 11; median z the lesioned side, i.e. to the left ear ( fig. 6 C, E, G). How- score DL freq 5.5, DLint 7.0, DLdur 4.0). These patients ever, the discrimination thresholds were elevated when showed normal discrimination thresholds for the same the test stimuli were presented contralesionally, i.e. to the acoustic cues when the signals were presented monau- right ear. The impairment was not as severe as in the cas- rally to either one of the two ears or – in the dichotic s/n es discussed earlier, but the mean results in different tests tests – to the ipsilesional ear (median of z scores for all
Hemispheric-Specific Auditory Audiol Neurotol 2008;13:123–144 133 Impairment Downloaded by: Universität Leipzig 139.18.89.136 - 10/9/2013 11:18:50 AM Audiogram 100 60–69 years 90 305 right 80 305 left 70 60 50 40 30 20 10
Hearing threshold (dB SPL) Hearing threshold 0 –10 0.125 0.25 0.5 124816 A Frequency (kHz)
Monaural Dichotic s/n 60–69 years 60–69 years 305 right 305 right 100.0 100.0 305 left 305 left 50.0 50.0
10.0 10.0 5.0 5.0
1.0 1.0 0.5 0.5 jn frequency difference (Hz) jn frequency difference Frequency (Hz) jn frequency difference Frequency
0.25 0.50 1.00 2.00 4.00 0.25 0.50 1.00 2.00 4.00 BCFrequency (kHz) Frequency (kHz)
18 Intensity 18 Intensity 16 16 14 14 12 12 10 10 8 8 6 6 4 4
jn intensity difference (dB) jn intensity difference 2 (dB) jn intensity difference 2 0 0 0.5 1.0 2.0 4.0 0.5 1.0 2.0 4.0 DEFrequency (kHz) Frequency (kHz)
200 200 Duration Duration 180 180 160 160 140 140 120 120 100 100 80 80 60 60 40 40
jn duration difference (ms) jn duration difference 20 (ms) jn duration difference 20 0 0 0.5 1.0 2.0 4.0 0.5 1.0 2.0 4.0 FGFrequency (kHz) Frequency (kHz)
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Downloaded by: Universität Leipzig 139.18.89.136 - 10/9/2013 11:18:50 AM tested features: 0; n = 11). Eight patients (patients 327, 341, C o n t r o l P a t i e n t s 448, 537, 522, 574, 577 and 662) with left temporal injuries Three groups of patients were studied with the same showed the same contralesional impaired performance set of psychoacoustic tests in order to evaluate the speci- under dichotic s/n stimulation and additionally impaired ficity of the test procedures. All these patients had lesions duration discrimination under monaural stimulus con- either close to the auditory cortex itself or to its afferents, ditions (fig. 8B; n = 8; median z score DL freq 5.0, DLint 6.0, but in all cases the lesions spared these structures.
DLdur mon ipsi 3.0, DL dur mon contra 4.0, DLdich ipsi 4.0, Lesion of the Occipital Lobe and the Basal and/or Cau-
DLdur dich contra 8.0). dal Temporal Lobe. One group included 14 patients suf- fering from infarctions of the posterior cerebral artery (6 left, 6 right, 2 bilateral) which had caused lesions of dif- Patients without Deficits in Auditory Discrimination ferent sizes enclosing areas posterior and inferior to the auditory cortex. These patients were afflicted with vari- Unilateral Lesion in the Domain of the Acoustic ous forms of central visual impairment like superior or Radiation inferior quadrantanopia or even hemianopia. Despite the Two more patients (patients 130 and 289) were inves- existence of serious neurological impairments, these pa- tigated, who also suffered from lesions in the area of the tients attained results that were normal for age in all au- left acoustic radiation, though much smaller and located ditory tests, regardless of the ear tested or the laterality of more medially and posteriorly than in the cases described the percept (fig. 9). Some threshold values were elevated, above. The patients were studied 42 and 1 month after the but since these occurred in an unsystematic manner, they insult, respectively. Despite the fact that in each of these were attributed to attention deficits. 2 the left auditory cortex seemed to have been cut off from Lesion of the Temporal Pole. Lesions restricted to the its direct thalamic input, they mastered all interaural, rostral pole of the temporal lobe are rare incidences. Four monaural and all dichotic s/n tests, irrespective of wheth- such cases, which showed lesions anterior of Heschl’s gy- er the test signals were presented to the left or to the right rus, could be explored in the present study. All of them ear ( table 3 ). One option would be that the left auditory performed equally well in discriminating frequency, in- cortex receives an auditory input from the contralateral tensity and signal duration under all test conditions. (right) auditory cortex through interhemispheric fibers Subcortical Lesions Adjacent to Auditory Structures. running in the corpus callosum (see ‘Discussion’). Six patients who suffered from lesions in the basal ganglia and/or the internal capsule were studied as well. In all patients neither the medial geniculate nucleus nor the acoustic radiation were affected. All 6 patients were ca- pable of discriminating frequency, intensity and tone du- F i g . 6 . Psychoacoustic data sheet for patient 305. The audiograms ration differences in the interaural and monaural as well for left (+ ) and right ear (y ) stimulation show elevated thresholds as in the dichotic s/n tests, irrespective of the side of sig- at frequencies 12 kHz, but rather good hearing at lower frequen- nal presentation ( fig. 9). cies ( A ). The mean threshold values (8 SD) for normal-hearing 60- to 69-year-old subjects are indicated by a black line [norma- tive data from Bungert-Kahl et al., 2004]. The just noticeable (jn) Discussion frequency difference limens for monaural ipsilesional (+ ) left and contralesional ( _ ) right ear stimulation ( B) and dichotic sipsi / ncontra (I ) and dichotic scontra /nipsi (y ) stimulation (C ). Intensity The present study aimed at an evaluation of the impact discrimination limens for monaural ipsilesional (left) and con- of unilateral lesions in cortical and subcortical auditory tralesional (right) stimulation ( D ), and dichotic s ipsi/n contra and structures on central auditory processing of the acoustic dichotic s contra /n ipsi stimulation ( E ) (symbols as in B , C ). Discrim- ination limens for signal duration measured with monaural (F ) parameters frequency, intensity and signal duration. The and dichotic s/n stimulation ( G ) (setup of the graph as in B , C ). brain anatomy of the patients investigated had been visu- Note that as in patients 178 and 448 (fig. 3, 4) all monaural tests alized by high resolution MRT scans, whereby a precise (B , D , F ) mostly yielded results in the range of age-matched con- correlation between lesions in central auditory structures trols. The same was true for most of the dichotic s/n tests with the and perceptual deficits could be established. The patients test signals presented to the ipsilesional (left) ear. Impaired per- formance in the dichotic discrimination tasks were consistently included in the study suffered from lesions in the right or found when the signals were presented contralaterally to the le- left auditory cortex or from interruptions to the left sion. acoustic radiation. In most patients, the lesions had no
Hemispheric-Specific Auditory Audiol Neurotol 2008;13:123–144 135 Impairment Downloaded by: Universität Leipzig 139.18.89.136 - 10/9/2013 11:18:50 AM Auditory Patient 305 Discrimination of basal acoustic parameters brainstem
Interaural f Monaural f Dichotics/n f Frequency 0/0/0 0/0/1 0/0/– 0/0/– 3/0/2 2/5/8
Interaural I Monaural I Dichotics/n I
Intensity F i g . 7 . Psychoacoustic data sheet for pa- 0/0/0/0 0/0/0/0 0/3/1/0 0/1/0/0 3/0/0/0 6/8/7/4 tient 305. All values are z scores indicating the deviation of the respective measure- ment from the mean values in 60- to 69- Interaural t Monaural t Dichotics/n t year-old normal-hearing subjects. Design Duration of the graph as in figure 3. Note that im- 0/0/–/– 0/1/0/1 0/0/–/– 0/–/–/– 1/0/0/0 5/3/3/4 paired discrimination for frequency, in- tensity, and duration differences were con- sistently found in the dichotic s/n tests with the signals presented to the right Ear/percept Left side Right side Left ear Right ear Left ear Right ear ear.
Frequency Intensity Duration Frequency Intensity Duration 20 20 18 18 16 16 14 14 12 12 10 10 Z score Z score 8 8 6 6 4 4 2 2 0 0 i i i i i i c c c c c c s/n s/n s/n s/n s/n s/n s/n s/n s/n s/n s/n s/n Monaural i Monaural i Monaural i Monaural i Monaural i Monaural i Monaural c Monaural c Monaural c Monaural c Monaural c Monaural c Dichotic Dichotic Dichotic Dichotic Dichotic ABDichotic Dichotic Dichotic Dichotic Dichotic Dichotic Dichotic
F i g . 8 . Summary graph for patients with contralateral auditory tion with signals presented contralesionally ( c ) and noise ipsi- impairment (n = 11) (A ) and patients who additionally showed lesionally (i ) revealed elevated thresholds (median of z scores: deficits in discrimination of monaurally presented duration dif- frequency = 5.0, intensity = 7.0, duration = 4.0). B In the ferences [n = 5; medians, 25 and 75% quartiles (box) ( B ), and the group of patients with left-hemispheric injuries the same contra- 90% interdecile ranges (vertical lines)]. A For all monaural as well lateral impairment was measured, and the discrimination limens as dichotic ipsilesional signal presentations the just noticeable dif- for monaurally presented duration differences were elevated as ference limens were mostly in the range of age-matched norma- well (median of z scores: frequency = 5.0, intensity = 6.0, du- tive data (in all tests medians of z scores are 0 and the 25 and 75% ration mon ipsi = 3.0, duration mon contra = 4.0, duration dich ipsi = quartiles hardly stand out against the median). Dichotic stimula- 4.0, duration dich contra = 8.0).
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Downloaded by: Universität Leipzig 139.18.89.136 - 10/9/2013 11:18:50 AM Basal ganglia/ Occipital lobe Temporal pole internal capsule f f i i t t f f i i t t f f i i t t 20 n = 14 n = 4 n = 7 18 16 14
F i g . 9 . Summary graph for patients with 12 lesions in the occipital lobe (n = 14), lesions 10 in the rostral pole of the temporal lobe Z score 8 (n = 4) and patients with lesions in the re- gion of the basal ganglia and internal cap- 6 sule sparing auditory structures [n = 7; 4 medians horizontal line, 25 and 75% quar- 2 tiles (box), and the 90% interdecile ranges (vertical lines)]. f = Frequency difference 0 i i i i i i i i i limens, i = intensity difference limens, c c c c c c c c c /n /n /n /n /n /n /n /n /n /n /n /n /n /n /n /n /n /n t = duration difference limens. All pa- i c i c i c i c i c i c i c i c i c tients mostly reached threshold values in the range of age-matched controls in in- teraural, monaural and dichotic s/n tests Dichotic s Dichotic s Dichotic s Dichotic s Dichotic s Dichotic s Dichotic s Dichotic s Dichotic s Dichotic s Dichotic s Dichotic s Dichotic s Dichotic s Dichotic s Dichotic s Dichotic s Dichotic s (median z scores = 0).
effect on the discrimination of acoustic signals presented In the patient investigated, unimpaired auditory per- monaurally to either ear independently of the parameter formance was observed in the interaural tests and in the varied. Also the interaural tests, which evaluated the abil- dichotic s/n tests when the test signals were presented ip- ity to discriminate lateralized from centralized sound silaterally to the lesion. Deficits in auditory discrimina- sources, gave normal results. tion manifested themselves in the dichotic s/n tests if and The discrimination thresholds in the monaural and only if the test signals were presented contralesionally. dichotic s/n tests on the one hand and in the interaural tests on the other hand can be quite different, and it is Dichotic s/n Tests for the Evaluation of Telencephalic plausible to relate these differences to distinct mecha- and Diencephalic Auditory Integrity nisms of auditory signal processing. These differences are The significance of the currently used dichotic s/n also linked to fundamentally different kinds of auditory tests, which help to reveal perceptual deficits not dis- percepts. In the monaural and in the dichotic s/n tests the cerned by monaural stimulation, can be particularly ap- subjects perceive the reference and the test signals as be- preciated if one considers the specific quality of the cen- ing different in either one of the three acoustic features tral auditory system, namely the fact that the cortical in- frequency, intensity or duration. The respective signals put itself is already the result of an extensive preprocessing are ‘localized’ at the stimulated ear. The percept induced in the auditory brainstem. One key feature of this prepro- in any of the interaural tests is that of a signal which ap- cessing is the integration of input from both ears, which pears to be ‘localized’ at different positions within the occurs at three levels of the afferent system: (i) the supe- head. The reference signals are centralized in the middle rior olivary complex, (ii) the nuclei of the lateral lemnis- of the head, while the test signals appear to be lateralized cus, and (iii) the inferior colliculus. All these processing on the interaural axis (stationary or moving) depending domains additionally establish commissural connections on the actual stimulus settings. In the latter tests, subjects [mammals: Cant, 1992; Irvine, 1992; nonhuman primates are not able to recognize which specific interaural feature and humans: Strominger, 1978; Nieuwenhyus et al., 1988; mismatch ( frequency, intensity, signal duration or Webster, 1992]. Neurophysiological recordings in various phase) causes the respective lateralized percept [Bun- mammalian species including primates showed that, as a gert-Kahl et al., 2004]. consequence of this binaural integration, the thalamo-
Hemispheric-Specific Auditory Audiol Neurotol 2008;13:123–144 137 Impairment Downloaded by: Universität Leipzig 139.18.89.136 - 10/9/2013 11:18:50 AM cortical afferents predominantly convey binaural infor- jects show only slightly diverging performance in dichotic mation [guinea pig: Rutkowski et al., 2000; cat: Middle- s/n and in monaural tests [Bungert-Kahl et al., 2004]. The brooks et al., 1980; Phillips and Irvine, 1983; primates: unimpaired central auditory system seems to be capable Imig and Morel, 1983; Reser et al., 2000]. In principle, this of preventing interferences between the nonmatching in- binaurality explains the preserved sensitivity for stimula- puts in the dichotic tests. Patients with acquired lesions in tion of either ear following a unilateral lesion in the audi- cortical or subcortical auditory structures, however, typi- tory cortex. Yet, on closer inspection, slightly different cally perform less well in the dichotic s/n tests, and sys- conditions for signal processing can be distinguished in tematic investigations disclosed a good match between le- the two hemispheres, mostly due to the imbalance of in- sions and specific deficits in different subtests. put organization. Recordings of cortical auditory evoked potentials [human: Celesia, 1976; nonhuman mammals: Lesion in the Auditory Cortex Kitzes, 1984; Reale et al., 1987; Popelar et al., 1994], and With the auditory cortex in one hemisphere lesioned, unilateral auditory cortex ablation [nonhuman primates: the imbalance between the ipsilateral and contralateral
Heffner and Heffner, 1989], as well as EEG and func- input to the remaining intact cortex became behaviorally tional magnetic resonance imaging studies in humans relevant in the dichotic s/n tests. In those cases, elevated [Scheffler et al., 1998; Woldorff et al., 1999; Jäncke et al., discrimination thresholds were found for ipsilesional 2002] produced evidence to suggest a ‘functional’ domi- noise presentation, i.e. when the test signals were present- nance of afferents crossing from either ear to the contra- ed contralateral to the lesioned auditory cortex. Inverse lateral cortex. Along these lines are reports which state stimulus conditions yielded thresholds that were normal faster signal transduction to the contralateral than to the for age, which supports the assumption that the relative ipsilateral cortical hemisphere and a stronger contralat- strength of the respective cortical input is crucial for au- eral cortical activation [Hall and Goldstein, 1968; Maj- ditory performance. During monaural stimulation, the kowski et al., 1971; Phillips and Irvine, 1979]. Similarly, ipsilateral input to the still functional auditory cortex unilateral electrical stimulation of the auditory cortex (in proved sufficient for an unimpaired auditory perfor- patients undergoing brain surgery) induced a perception mance, but adding the noise to the other ear (fig. 10B) of sound in the ear contralateral to the side of stimulation caused a central auditory masking [Zwislocki, 1972; Mills [Penfield and Perot, 1963]. et al., 1996] of the signal, which led to an elevation of dis- In the present study, we made use of the preponderance crimination thresholds. Similarly, contralateral masking of crossed projections to the auditory cortex by using effects were shown by the use of dichotic stimulation in dichotic s/n tests for the identification of hemisphere-spe- cats that underwent a unilateral ablation of the auditory cific lesions. In these tests, the signals to be discriminated cortex [Cranford, 1975]. were presented to one ear and paired with noise pulses si- In the patients investigated here, this contralateral im- multaneously presented to the other ear (fig. 10 ). This pairment was evident if either the right or the left audi- stimulus configuration generates an uneven, side-specific tory cortex was affected by the lesion, and it was seen in activation in each of the two auditory cortices as shown in the discrimination thresholds for all three acoustic pa- figure 10 A for the undamaged brain. Each auditory cortex rameters – frequency, intensity and tone duration. receives systemic input from three distinct sources: the Though not easy to seize and much less to grasp, our ipsilateral acoustic radiation conveys auditory input which data also point to systematic differences between the ef- originates (i) from the contralateral and (ii) from the ipsi- fects of auditory cortex lesions in the left and the right lateral ear, and (iii) in its final path an additional input hemisphere. Following right hemispheric lesions, audi- mediated through transcallosal auditory connections. tory impairments tend to be more uniform, while left Since the strengths of the respective projections differ, the hemispheric lesions result in more differentiated patterns dichotic s/n stimulation will establish a dominant repre- of auditory deficiencies. This shall be exemplified by a sentation of the pure-tone signals in the auditory cortex comparison of the data from patients 178 and 448, who contralateral to the receiving ear and a weaker representa- had lesions in the right and left auditory cortices, respec- tion of the noise bursts received through the ipsilateral tively. While patient 178 showed pronounced deficits in ear. An inverse weighting of the respective signal and the dichotic s/n tests ( fig. 2, 3 ), patient 448 additionally noise input comes to effect in the auditory cortex ipsilat- had deficits in the processing of temporal information eral to the ‘signal ear’. Despite these differences in input under monaural test conditions ( fig. 4 ). Thus, left cortical strengths to either auditory cortex, normal-hearing sub- lesions might additionally affect higher-order cortical
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Downloaded by: Universität Leipzig 139.18.89.136 - 10/9/2013 11:18:50 AM A Mechanism of signal processing under dichotic s/n presentation
Cortical AC AC Signalcontra Noisecontra representation Noiseipsi Signalipsi Signal/Noise F i g . 1 0 . Simplified scheme of the main af- Central callosal Noise/Signalcallosal projections ferent projections from both ears to the au- ditory cortex (AC) of each hemisphere Ear Noise Signal during dichotic s/n stimulation. A Intact central auditory system. Ear: test signals (signal) and noise bursts (noise), separate- B Lesion of auditory cortex/contralateral auditory deficit in dichotic s/n tests ly presented to the two ears, converge at the level of the auditory brainstem estab- Cortical AC Noisecontra lishing a binaural input to either AC. Cen- representation Signalipsi tral projections: the AC input from the Central ipsilateral, the contralateral ear, and the projections contralateral AC is indicated by arrows. Ear Cortical representation: the supposed Noise Signal strength of the respective input is indicat- ed by the size of the letters in order to vi- Lesion of acoustic radiation left and transcallosal fibers/ sualize the imbalance of the converging C contralateral auditory deficit in dichotic s/n tests afferents to the two ACs. B Lesion of the AC of the right hemisphere (or left hemi- Cortical AC AC sphere, respectively) causes threshold ele- representation Noisecontra vations in the dichotic s/n tests when the Signalipsi test signals are presented contralaterally to Central the side of lesion because the remaining projections AC of the other hemisphere is incapable of Ear extracting feature variations in the pres- Noise Signal ence of the dominant noise input. C Inter- ruption to the acoustic radiation together D Lesion of acoustic radiation/no auditory deficit in dichotic s/n tests with that of the transcallosal auditory fi- Cortical bers has the same overall effect as a direct AC AC Noise lesion of AC areas. D Interruption to the representation contra Signalipsi acoustic radiation alone does not cause Central Signal/Noisecallosal such deficits in dichotic s/n tests. Appar- projections ently an AC deprived only of its direct tha- lamic input can still contribute to auditory Ear Noise Signal processing through transcallosal auditory connections.
processing domains devoted to processing of temporal agreement with our results, this study reported signifi- information. This is in agreement with earlier investiga- cantly impaired signal discrimination associated with tions of hemispheric asymmetries in which a left-hemi- left-hemispheric lesions. After right-hemispheric lesions, spheric dominance for the processing of temporal cues however, the respective data showed only mild threshold was hypothesized [Schwartz and Tallal, 1980; Robin et elevations. Thompson and Abel [1992] had confined al., 1990; Zatorre and Belin, 2001; Tervaniemi and Hug- themselves to contralesional signal presentations and thus dahl, 2003; Schönwiesner et al., 2005]. failed to assess reference values which would have enabled Earlier investigations in patients with acquired brain a more detailed characterization of patient performance. lesions made use of various forms of dichotic tests for the The study also lacked detailed specifications of the pa- evaluation of impaired auditory performance. Dichotic tients’ lesions such as exact position, size and etiology. s/n tests, comparable to those used here, were utilized by Contralateral deficits related to lesions of cortical au- Thompson and Abel [1992] for the assessment of discrim- ditory areas or of the acoustic radiation had also been ination thresholds of signal frequency and duration. In shown by the use of dichotically presented click trains
Hemispheric-Specific Auditory Audiol Neurotol 2008;13:123–144 139 Impairment Downloaded by: Universität Leipzig 139.18.89.136 - 10/9/2013 11:18:50 AM [Blaettner et al., 1989]. Musiek et al. [1994] summarized immediate lesion of the auditory cortex. The respective a larger number of cases from neurology, all with lesions contralateral impairments in the dichotic s/n tests have in those telencephalic areas which are thought to contrib- to be expected in cases where the auditory cortex had ute to auditory processing, e.g. superior temporal gyrus, been deprived of all of its auditory input, both the ascend- insula, corpus callosum. When investigated with dich- ing thalamic and the transcallosal ones. Under these con- otic speech and consonant-vowel tests, these patients in- ditions, the auditory cortex (although itself undamaged) deed showed impaired perception of contralesionally is incapable of contributing to signal processing ( fig. presented signals [see also Kimura, 1961; Berlin et al., 10C). A comprehensive analysis of the lesions in the re- 1972; Efron and Crandall, 1983]. Most of the studies that spective patients is in accordance with this notion. In pa- employed dichotic speech tests mainly explored the ef- tients 214, 228, 305, 327 and 522, the tissue necrosis ex- fects of left-hemispheric lesions on the processing of tended from the posterior thalamus (including the me- acoustic information presented to either ear [Kimura, dial geniculate nucleus) to the retrolenticular portion of 1967; Zurif and Ramier, 1972; Speaks et al., 1975; Musiek the internal capsule (containing the acoustic radiation) and Pinheiro, 1985]. Yet, the close link between auditory [Mesulam and Pandya, 1973; Rademacher et al., 2002] areas and speech areas in the left cortical hemisphere and up to the external capsule, where the transcallosal does not allow an unequivocal decision as to whether a auditory fibers presumably pass through [Pandya and specific impairment was due to an auditory-perceptual Rosene, 1993]. In patient 046, the cortical band of deficit or an indication of an aphasic disturbance [Swish- Heschl’s gyrus was likewise left intact, but the underlying er and Hirsh, 1972; Warren and Gardner, 1995]. gyral stalk of the superior temporal gyrus was complete- ly necrotic. A common feature of the subcortical lesions Deafferented Auditory Cortex in these 4 patients was the inclusion of the acoustic ra- A subcortical lesion of the acoustic radiation deprives diation and parts of the external capsule or the temporal the auditory cortex of its ipsilateral thalamic afferents. isthmus. This is consistent with the notion of a complete This may or may not occur in association with an inter- deafferentation of the primary auditory cortex. ruption to the transcallosal fibers which interconnect the Two more patients (130 and 289), who also suffered primary and secondary auditory cortices of the two hemi- from lesions of the acoustic radiation, showed a very dif- spheres (fig. 10C, D). Referring to data from nonhuman ferent performance in the psychoacoustic tests. It is not primates, the transcallosal fibers traverse through the ex- surprising that the dichotic s/n tests yielded results that ternal capsule before they merge with the ascending thal- were in the range of age-matched normal controls when amocortical auditory fibers in more distal parts of the the test tones were presented ipsilesionally (i.e. contralat- acoustic radiation to form a patchy pattern of thalamic erally to the intact acoustic radiation). A remarkable find- afferents and transcallosal fibers within the auditory cor- ing, however, is the equally good performance when the tex [Cipolloni and Pandya, 1985; Pandya and Rosene, test signals were presented contralesionally. In these cas- 1993]. In humans, neither the exact course of the trans- es, the imbalance between the strength of afferents arising callosal auditory fibers nor the location where they join from the ipsi- and contralateral ear did not take effect. the ascending thalamocortical fibers is known [Springer There are two possible explanations for this result: and Gazzaniga, 1975; Sugishita et al., 1995; Pollmann et (1) The hemorrhage-induced pseudocystic transfor- al., 2002]. In contrast, the course of the acoustic radiation mation of the lesioned tissue was incomplete, leaving [Rademacher et al., 2002] and the pattern of fibers enter- parts of the fibers of the acoustic radiation intact. Those ing Heschl’s gyrus [Pfeiffer, 1920] are well documented. could possibly pass on enough auditory information to Thus it was impossible to distinguish in the present study the cortex for mastering the dichotic s/n tests. Addition- (solely relying on the sites of the respective brain lesions) ally, a posttraumatic increase in the efficiency of signal between patients whose auditory cortices were deprived transduction in the remaining fibers or cortical reorga- either of their thalamic and transcallosal afferents or nization might have improved the situation. The latter only of their thalamic afferents. Still, the performances of assumption is supported by reports of symmetric activa- patients with lesions in the acoustic radiation show a bi- tions in both auditory cortices about 4 weeks after uni- partition that is consistent with the assumption of such a lateral deafening in experimental animals [Fujiki et al., differentiation. In 6 patients (patients 046, 214, 228, 305, 1998; Scheffler et al., 1998], the modification of synaptic 327 and 522), the performance in the psychoacoustic tests efficiency induced by the transcription of early genes was comparable to that observed in the presence of an [Kaczmarek and Chaudhuri, 1997], synaptogenesis [Jain
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Downloaded by: Universität Leipzig 139.18.89.136 - 10/9/2013 11:18:50 AM et al., 2000], and the recruitment of modified cortical net- dya, 1998] suggests a possible modulatory effect of these works [Nudo and Friel, 1999]. structures on auditory performance. The basal ganglia (2) A closer inspection of the MRI data showed that in are closely related to cognitive and attention-guided pro- both patients a hemorrhage in the posterior thalamus had cesses [Damasio et al., 1980] including speech processing resulted in tissue necrosis located more medially and pos- [Viader et al., 1987; Rees, 1998]. Also, it has been shown teriorly than the lesions in the patients described above. that the auditory cortex directly projects to the basal gan- The necroses extended to the medial geniculate nucleus glia [Reale and Imig, 1983; Yeterian and Pandya, 1998; and the proximal portion of the acoustic radiation, but Beneyto and Prieto, 2001]. Our results show that, if the spared the external capsule. It is tempting to assume that lesions are restricted up to the crus posterior of the stria- in both patients the lesion only disrupted the thalamocor- tum, they had no effect on auditory processing. Such le- tical afferents, but left the transcallosal auditory connec- sions appear not to have affected the pars retrolenticu- tions intact ( fig. 10 D). This interpretation would be con- laris, that portion of the internal capsule which hosts the sistent with an apparent peculiarity of cortical auditory acoustic radiation [Rademacher et al., 2002]. processing, namely the close cooperation between the au- The performance of these control patients was normal ditory cortices of both hemispheres. Possibly both audi- for age in all interaural, monaural, and dichotic s/n tests. tory cortices in conjunction could provide enough pro- These results do not support the assumption of unspe- cessing power to cope with the different input conditions cific ‘neighborhood effects’ of the described subcortical in the dichotic s/n tests. The mostly unimpaired auditory and cortical lesions on auditory processing. It seems that performance in these 2 patients thus challenges the con- the direct damage to auditory structures is the precondi- cept of the functional significance of the direct thalamic tion for an impact on auditory processing. input to the auditory cortices of either hemisphere. Conclusion: What to Do with the Binaural Input to Lesions Sparing Auditory Structures Either Auditory Cortex? To show the specificity of the tests designed for the Dichotic s/n headphone stimulation, which helped to present study, 25 additional patients were investigated disclose the hemisphere-specific deficits in auditory pro- who also had lesions in the forebrain, which, however, did cessing, is an artificial stimulus condition and very dis- not affect auditory structures. tinct from sounds perceived in the free field. Notably, the Fourteen patients suffered from a stroke of the poste- fact that both ears were stimulated with disjunctive sig- rior cerebral artery, and they will exemplify possible un- nals permitted to evaluate the effect of signal convergence specific effects of extended cortical lesions posterior and in the intact and in the lesioned auditory cortex. In addi- inferior to the auditory cortex on the discrimination of tion to these immediate results, the performance in the acoustic information. None of the tested patients showed dichotic s/n tests and that in the interaural tests shed light a contralateral deficit as revealed by the dichotic s/n tests. on some peculiarities of the functional organization of Four patients with lesions of the rostral pole of the the auditory cortices. temporal lobe were studied to evaluate possible effects of One basic question that arises relates to the functional restricted lesions anterior to the auditory cortex. Al- significance of the binaural input to the primary audi- though in these cases the lesions were rather close to the tory cortical areas of either side. This issue has to be stud- auditory cortex, all patients were able to master all dis- ied with respect to both the discrimination of acoustic crimination tests including the dichotic s/n tests with features and the localization (or lateralization) of sound stimulus presentations to either ear. We have to empha- sources. In these respects, it is necessary to evaluate the size, however, that the lesions in 3 of the 4 patients in this settings of ipsi- and contralateral cortical input under group had a different etiology than most of the subjects natural hearing conditions. For free-field stimulation, investigated in this study (patients 236, 252 and 761; ta- and considering the spectrotemporally complex struc- ble 2). They were included because of the rarity of focal ture of naturally occurring sounds, the signals that arrive lesions at the frontal pole of the temporal lobe. at both ears can differ in some respect (depending on the Seven more patients were selected because they had laterality of the source), but will still bear a certain degree lesions in the striatum including the surrounded capsules of congruency. of the left hemisphere. The fact that projections from the The differences between the input signals at the two auditory cortex terminate in the body and the tail of the ears matter with respect to the localization of sound sourc- caudate nucleus [nonhuman primates: Yeterian and Pan- es. To appreciate this condition, especially in view of the
Hemispheric-Specific Auditory Audiol Neurotol 2008;13:123–144 141 Impairment Downloaded by: Universität Leipzig 139.18.89.136 - 10/9/2013 11:18:50 AM functional organization and the phylogeny of the central igin of two divergent, though not completely alternative auditory system, it is necessary to evaluate intrinsic differ- developments as seen in extant mammals and specifical- ences between the auditory system on the one hand and the ly in primates. One aspect of the development may be the visual and the somatosensory systems on the other hand. establishment of cooperation between the auditory corti- Unlike in the latter systems, in the auditory system the lo- ces in both hemispheres to increase the processing power cation (or direction) of the signal source is not mapped di- of the cortical system. This notion is supported by the rectly onto the sensory organ. This is mostly due to the long abundance of interhemispheric reciprocal connections of wavelength of airborne sound waves in the biologically sig- the respective primary and secondary auditory areas nificant frequency range up to about 10 kHz [Colburn et al., [Fitzpatrick and Imig, 1980; Kaas and Hackett, 2000]. 1987]. However, it is reasonable to assume that the ability to The second aspect of the bilaterally organized processing localize sound sources was a key requirement throughout of auditory information is the possibility for functional auditory system phylogeny. The auditory brainstem with its segregations in both hemispheres. The (mostly) left- multitude of monaural and binaural nuclei can be inter- hemispheric dominance in human speech processing preted as an integrative system for neural computation of and the right-hemispheric dominance in the processing spatial acoustic information. From in vivo electrophysiol- of spectral information are examples for such functional ogy we know that such spatial information is already avail- segregations. In this respect, the presently available data able at the level of the superior colliculus [Middlebrooks are clear about the involvement of tertiary auditory cor- and Knudsen, 1984], i.e. the respective signal processing tex areas and auditory association cortices. But it might takes place at lower stages in the brainstem. The auditory well be the case that primary and secondary cortex areas cortex, in part, seems to fall back on this brainstem process- in both hemispheres also show the respective adapta- ing [Furst et al., 2000; review: Middlebrooks et al., 2002], tions, or are subject to an immediate, ipsilateral top-down but primary cortical areas apparently play a role in the lo- influence by the above-mentioned cortical fields. calization task as well [Zatorre and Penhune, 2001; Zatorre et al., 2002a, b; Grube et al., 2005]. We still do not know the algorithm of the cortical representation of acoustic space, A c k n o w l e d g m e n t s but there is accumulating experimental evidence that it is basically a bilateral organization though with a dominance This work is supported by Deutsche Forschungsgemeinschaft, Cr 43/13-1, Cr 43/13-2, VW I/70 204. 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