sign in sign up
<<
Home , Lateral lemniscus, Trapezoid body

52252ournal ofNeurology, Neurosurgery, and Psychiatry 1997;62:522-526 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.62.5.522 on 1 May 1997. Downloaded from SHORT REPORT

Sound movement detection deficit due to a lesion

T D Griffiths, D Bates, A Rees, C Witton, A Gholkar, G G R Green

Abstract lesion involving the , suggesting Auditory psychophysical testing was car- that convergence at the level of the superior ried out on a patient with a central pon- olive is needed for human sound movement tine lesion involving the trapezoid body, analysis. who presented with a deficit in sound localisation and sound movement detec- tion. A deficit in the analysis of time and Methods intensity differences between the was CASE REPORT found, which would explain the deficit in The patient presented at the age of 45 with detection of sound movement. The recent symptoms. She described diffi- impaired detection of sound movement, culty with making out some speech sounds, due to a lesion interfering with conver- particularly in crowded rooms, and a difficulty gence of auditory information at the with sound localisation such that she had superior olive, suggests this structure to become unable to detect which of three well be critical for human sound movement separated telephones in her office was ringing. analysis. The patient also had difficulty with the per- ception of moving sounds. For example, she (7 Neurol Neurosurg Psychiatry 1997;62:522-526) was unable to detect which way a train was travelling when she was standing on a plat- Department of form, on the basis of sound alone. She had a Physiological Sciences, Keywords: sound; sound movement; brainstem; history of more than 10 years of right sided Newcastle University human; lesion headaches and more recent right sided tinni- Medical School, Newcastle upon Tyne, tus, in addition to episodes of rotatory vertigo. The analysis of movement in the sys- NE2 4HH, UK auditory Neurological examination was remarkable http://jnnp.bmj.com/ T D Griffiths tem requires changes in the phase and ampli- only for the presence of nystagmus on right A Rees C Witton tude of the sounds arriving at the two ears to lateral gaze. G G R Green be compared. Both processes depend on the Brain MRI with gadolinium showed an Department of Clinical convergence of information from the ears. enhancing lesion in the central (fig 2), Neuroscience, This convergence first occurs at the superior between the dorsal pontine and Newcastle University olive, where the input from the ipsilateral ventral pons and extending rostrally, but not Medical School, converges Newcastle upon Tyne, with that from the as far as the . Angiography of the pos- NE2 4HH, UK contralateral cochlear nucleus, relayed via the terior circulation was normal; the lesion was on September 28, 2021 by guest. Protected copyright. T D Griffiths trapezoid body (fig 1). Convergence also thought to be a capillary vascular malforma- D Bates occurs higher in the pathway at the level of the tion. Welicome Department colliculi. Neurophysiological studies in ani- of Cognitive Neurology, Institute of mals have shown that the cells in the medial PSYCHOPHYSICAL TESTING Neurology, 12 Queen superior olive (MSO) respond to timing or Auditory testing was carried out with com- Square, London, phase differences between the ears in a linear puter generated stimuli presented over head- WC1N 3BG, UK T D Griffiths fashion,1 2 whereas cells at the level of the infe- phones in a sound proofed room. The tests Neuroradiology rior colliculus show non-linearities consistent with modulated sounds used a two alternative Department, with a selective response to sound movement.3 forced choice procedure, with a pure tone ref- Newcastle General Selective responses to sound movement have erence interval with at least 10 trials per point Hospital, Westgate Rd, also been shown in animals in the superior col- and at least five stimulus levels. Newcastle upon Tyne, NE4 6BE, UK liculus,4 primary ,5 6 7 and in A Gholkar humans in the multimodal cortex.8 Lesions Correspondence to: producing deficits in the detection of sound Results Dr T D Griffiths, Department of Physiological movement have not previously been reported PSYCHOPHYSICAL ASSESSMENT Sciences, Newcastle in humans, although we have recently Pure tone and fixed interaural phase difference University Medical School, a a Newcastle upon Tyne, reported patient with right hemispheric detection NE2 4HH,UK. stroke and a deficit in the detection of phase Pure tone thresholds disclosed a low frequency Received 11 June 1996 and amplitude changes simulating motion.9 sensorineural hearing loss of 35 dB on the left and in final revised form 21 January 1997 We report here a patient with a deficit in and 25 dB on the right at 500 Hz (fig 3). Accepted 23 January 1997 sound movement analysis due to a brainstem These losses were corrected for in the other Sound movement detection deficit due to a brainstem lesion 523 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.62.5.522 on 1 May 1997. Downloaded from Cortex L R

MGN

SC A -.

IC IC

A

Lateral

DCN DCN A A A LSO MSO MSO LSO MNTB MNTB A. VCN A A ...... -- ... i i A -A.VCN

A Cochlea Cochlea Trapezoid body Figure 1 Simplified diagram of the auditory pathway showing the convergence of the inputfrom both ears at the right sided brainstem auditory nucleii. This is based primarily on pathways describedfor the cat and other mammals'4 although anatomical differences between species (including humans) are described'5 16 (J K Moore, personal communication). In particular, there is debate about the relative importance of the pathway via the medial nucleus of the trapezoid body (MNTB) and lateral superior olive (LSO) in humans. All connections would be reflected in the midline. The medial superior olive (MSO) is shown to be the first point at which binaural convergence occurs via the trapezoid body. Convergence also occurs at higher levels, including the level ofthe nucleus of the (not shown) and (IC). The diagram shows a ventral pathway, via the (VCN), trapezoid body, and MSO, thought to be important in animals for the analysis ofspatial information. A dorsal pathway, via the (DCN) and IC, is also shown, which is involved in animals in the analysis ofcomplex waveforms. MGB = medial geniculate body, SC = .

psychophysical tests by using sensation levels mean of 180 for untrained controls. A further http://jnnp.bmj.com/ to match the stimulus at each , and addi- test was carried out to check whether the tionally checking that the binaurally presented patient was using phase differences between 500 Hz tones used in the other tests produced the ears, or was simply detecting the frequency a midline sound image. The threshold for modulation produced by the phase changes detection of a fixed phase difference between considered at either ear alone. This was done the ears at 500 Hz was 2.250 for a sound by playing the same phase modulated sound

which seemed to move to the right and 3.450 into the right or the left ear without a tone in on September 28, 2021 by guest. Protected copyright. for a sound which seemed to move to the left, the opposite ear for comparison. The patient which are within normal limits.'0 However, the performed at chance level on either side up to a patient found the task difficult and needed modulation depth of 1000, in the same way as repeated trials to achieve these normal values. normal listeners, confirming that she was using phase differences between the ears to Interaural phase modulation detection (sinusoidal detect the IPM stimulus. and ramp) Further testing was carried out with another Detection of changes in the phase or timing 500 Hz stimulus which contained a phase between the ears is used at low frequency to ramp, such that the phase advanced in one ear detect sound movement. Figure 4 shows the as it was delayed in the other ear. This stimulus psychophysical function for detection of a contains identical phase changes to a sound sound in which the phase is constantly moving in an arc around the head in one direc- changed between the ears: sinusoidal interau- tion, and was used as a more "physiological" ral phase modulation (IPM). The stimulus is stimulus than one moving from side to side, in perceived as a sound which moves from side to which repetition of apparent sound source side by normal observers, and was used as a positions could provide an extra cue. The more exacting test of the analysis of differ- patient was unable to perceive sound move- ences in phase between the ears. The patient ment during presentation of such a ramp over was able to perceive this stimulus as sound 300 ms or 500 ms in either direction, even movement, and had a detection threshold of when the magnitude of the phase change was

240 (by Weibull analysis) compared with a equivalent to 1800 . Figure 5 shows the perfor- 524 Griffiths, Bates, Rees, Witton, Gholkar, Green Figure 2 Tl weighted gadolinium enhanced J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.62.5.522 on 1 May 1997. Downloaded from MRI. (A) Transverse section at level ofthe midpons showing the central location of the lesion. (B) Midsagittal section showing lesion to extend rostrally to a point below the midbrain. cJ L-,aL) o O (-)

20

O0 0 10 20 30 40 50 Modulation depth (0) Figure 4 Psychophysicalfunction showing detection of interaural phase modulation (IPM) as a function of modulation depth expressed as degrees. Thefunctionfor the patient is plotted using closed circles. Also shown are mean (SEM) data for six controls (four normal controls and two with peripheral neurological disorders, mean age 60, range 43-77). For the IPM stimulus the phase is advanced in one ear as it is delayed in the other sinusoidally with a rate of2Hz. Carrierfrequency 500 Hz; sensation level 50 dB.

100-

80-

,, 60 60 >t~ ~

- 401

20 http://jnnp.bmj.com/

0 0 50 100 150 200 m Ramp excursion (0) (I)

m 5 40 Figure Psychophysicalfunction showing detection of a 500 ms interaural phase ramp, simulating motion in an arc around the as a > 50 head, plotted function ofphase change a) in degrees. The patient (O) was unable to detect any on September 28, 2021 by guest. Protected copyright. stimulus as =' 60 movement, whereas the four control subject curves (0; mean age 35, range 22-45) show a threshold phase shift of 43 for movement detection. The task was a 70 control I found easy by subjects. Carrierfrequency 500 Hz. 80 90 _ rier rates of 500 Hz and 3 kHz. This stimulus is one in which the 100 amplitude in one ear is 250 500 1000 2000 4000 8000 increased as it is decreased in the other ear in a Frequency (Hz) sinusoidal fashion, giving a perception of Figure 3 Pure tone audiograin ofpatient. Hearing levels sound movement from side to side as in the shown as O and (right) 0 (left). IPM stimulus. The threshold modulation depth was 30% at both carrier rates, which is high (compared with less than 10% in three mance of the patient compared with normal untrained normal controls aged over 50). controls for the detection of the 500 ms ramp. Matchedfrequency and amplitude modulated con- Interaural amplitude modulation detection trol stimuli Interaural amplitude modulation (IAM), Control stimuli were used in which the fre- which is a cue for the analysis of sound move- quency changes for the IPM condition and the ment which is not restricted to low frequencies amplitude for the IAM like changes condition phase cues, was also examined, at two car- were identical at the two ears. These condi- Sound movement detection deficit due to a brainstem lesion 525

tions were used to check that the deficit in This would provide a mechanism for preserva- J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.62.5.522 on 1 May 1997. Downloaded from detection of differences in the waveform tion of fixed lateralisation, as would any resid- between the ears was specific, and not due to a ual function in the trapezoid body. Lesion more general deficit in detecting changes in studies in the cat show impaired auditory sound over time. The threshold modulation localisation due to trapezoid body lesions,'2 13 depths for each condition were normal at less with only small increases in spatial discrimina- than 2 Hz for the frequency condition and less tion ability for discrete lesions confined to the than 15% for the amplitude condition (2 Hz trapezoid body. modulation rate and 500 Hz carrier). Convergence at the level of the colliculi and residual trapezoid body function might also be expected to allow preservation of detection of Discussion sound movement, a function ascribed to cells PSYCHOPHYSICAL DEFICIT in the midbrain.34 . This is not the case, and The psychophysical assessment showed a mild the pronounced deficit in detection of sound asymmetric hearing loss at 500 Hz. The movement in this patient with disrupted supe- degree of loss and degree of asymmetry are at a rior olive input is in accord with the idea that level which is lower than that at which deficits coding of phase differences needs to occur at in interaural timing detection have been this level to allow analysis of movement. shown," although this has not been investi- Whether specific movement analysis also gated for the degree of hearing loss shown by occurs at the level of the superior olive is this patient. A contribution from the hearing unclear; some non-linearities occur in animal loss and asymmetry to the deficit is still possi- recording work (MN Semple, MW Spitzer, ble, however. There was a mild impairment in personal communication) but not to the same the detection of fixed timing differences extent as in the inferior colliculus, where between the ears shown by the difficulty with analysis of sound movement is better estab- fixed phase difference detection. Such diffi- lished.3 culty would contribute to the sound localisa- tion deficit, although we were surprised not to find a more pronounced deficit in view of the Conclusion symptoms described. More strikingly, deficits This patient with a lesion involving the trape- in the detection of varying timing differences zoid body, has a dissociated deficit in spatial between the ears were brought out by the analysis, particularly sound movement, with ramp but not the sinusoidal interaural phase preservation of analysis of temporal sound fea- stimulus. The ramp stimulus may be more dif- tures. This is in accord with the idea that spatial ficult to detect because in each presentation a and temporal analysis of sound is separated phase transition occurs in one direction only, early in the human auditory pathway, as in whereas with the sinusoidal phase modulated other mammals. The convergence of input stimulus a phase transition occurs in both from the two ears via the trapezoid body is directions. This difference in the stimuli might important for the spatial pathway. Such provide an amplification of any subtle fixed deficits are not normally assessed in patients phase detection deficit when a moving stimu- with brainstem lesions, and it will be of con-

lus is used. Alternatively, the patient may have siderable interest to see if other patients with http://jnnp.bmj.com/ a deficit in the detection of non-linearities lesions involving the auditory pathway show related to sound movement which would not similar deficits. be predicted by fixed spatial performance. The TDG is a Wellcome research training fellow and CW an MRC patient also has a deficit in the detection of student. varying amplitude differences between the ears shown by the impaired detection of sinusoidal amplitude differences. Both phase and ampli- 1 Semple MN. Dynamic alteration of neural tuning to binaural cues: single unit responses to simulated auditory motion. on September 28, 2021 by guest. Protected copyright. tude deficits would contribute to the sound Antwerp, Belgium: European Acoustics Association Convention, 1996. movement detection deficit. The normal per- 2 Spitzer MW, Semple MN. Responses to time-varying inter- formance in detection of sinusoidal IPM, and aural phase disparity in gerbil superior olive: evidence for hierarchical processing [abstract]. J7 Neurosci 1992; of binaural frequency and amplitude modula- 18:149. tion, argue against a non-specific deficit in 3 Spitzer MW, Semple MN. Responses of inferior colliculus neurons to time-varying interaural phase disparity: effects psychophysical performance, or general deficit of shifting the locus of virtual motion. J Neurophysiol in the analysis of auditory timing information. 1993;69: 1245-63. 4 Raushecker JP, Harris LR. Auditory and visual neurons in the cat's superior colliculus selective for the direction of ANATOMICAL AND PHYSIOLOGICAL BASIS OF apparent motion stimuli. Brain Res 1989;490:56-63. DEFICIT 5 Stumpf E, Toronchuk JM, Cynader MS. Neurons in cat primary auditory cortex sensitive to correlates of auditory We suggest that the deficit in detection of motion in three-dimensional space. Exp Brain Res 1991; sound movement in 88:158-68. this patient is due to the 6 Ahissar M, Ahissar E, Bergman H, Vaadia E. Encoding of lesion involving the trapezoid body, the tract sound source location and movement: activity of single which carries crossed neurons and interactions between adjacent neurons in auditory information the monkey auditory cortex. J Neurophysiol 1992;67: from one side to allow convergence with the 203-15. from the other side 7 Toronchuk JM, Stumpf E, Cynader MS. Auditory cortex auditory information at the neurons sensitive to correlates of auditory motion: under- level of the superior olive (fig 1). The lateral lying mechanisms. Exp Brain Res 1992;88:169-80. in the lateral lem- 8 Griffiths TD, Bench CJ, Frackowiak RSJ. Cortical areas in ascending auditory pathway man selectively activated by apparent sound movement. niscus, and higher level convergence in the Curr Biol 1994;4:892-5. at 9 Griffiths TD, Rees A, Witton C, Shakir RA, Henning GB, pathway, including the level of the inferior Green GGR. Evidence for a sound movement centre in and superior colliculi, are spared by the lesion. the human cerebral cortex. Nature 1996;383:425-7. 526 Griffiths, Bates, Rees, Witton, Gholkar, Green

10 Blauert J. Spatial hearing. The psychophysics of human sound tem of the cat. Brain Res 1974;82:13-26. J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.62.5.522 on 1 May 1997. Downloaded from localisation. Cambridge, MA: MIT Press, 1983. 14 Irvine DRF. The auditory brainstem. A review of the structure 11 Hausler R, Colburn S, Marr E. Sound localisation in sub- and function of the auditory brainstem processing mecha- jects with impaired hearing. Acta Otolaryngol 1983; nisms. Berlin: Springer-Verlag, 1986. (suppi 400):1-62. 15 Moore JK, Moore RY. A comparitive study of the superior 12 Casseday JH, Neff WD. Auditory localisation: role of the olivary complex in the primate brain. Folia Primatol auditory pathways in brainstem of the cat. Neurophysiol (Basel) 1971;16:35-51. 1975;38:842-58. 16 Moore JK. The human brainstem auditory pathway. In: 13 Moore CN, Casseday JH, Neff WD. Sound localisation: Jackier RK, Brackmann DE, eds. Neurotology. St Louis: the role of the commisural pathwaysof the auditory sys- Mosby, 1994. http://jnnp.bmj.com/ on September 28, 2021 by guest. Protected copyright.