NEUROBIOLOGY OF LANGUAGE
Edited by GREGORY HICKOK Department of Cognitive Sciences, University of California, Irvine, CA, USA
STEVEN L. SMALL Department of Neurology, University of California, Irvine, CA, USA
AMSTERDAM • BOSTON • HEIDELBERG • LONDON NEW YORK • OXFORD • PARIS • SAN DIEGO SAN FRANCISCO • SINGAPORE • SYDNEY • TOKYO Academic Press is an imprint of Elsevier SECTION D
LARGE-SCALE MODELS CHAPTER 27 The Dual Loop Model in Language Cornelius Weiller, Tobias Bormann, Dorothee Kuemmerer, Mariachristina Musso and Michel Rijntjes Department of Neurology and Clinical Neuroscience, University Hospital Freiburg, Freiburg, Germany
The idea of two parallel streams to process language This interaction is accomplished through two principal seems almost ancient. For instance, Herder distin- routes. The route for the “direct” interaction of Broca’s guished a more automatic production route from a and Wernicke’s area would represent “sensorimotor close association of language with “self-consciousness” mapping” and produce the so-called Wortbegriff (Herder, 1772). The idea of conceptual representations (translated as “word-concept” or “word-form”) (DeWitt independent of linguistic representations is commonly & Rauschecker, 2013) as an intrinsic integration of sen- attributed to Lichtheim (1885), which may be due to sory and motor aspects of the word, learned during his invention of the famous house diagram. Yet in his development in early age through imitation and that is 1874 treatise Wernicke notes, “thinking and speaking later used to produce speech. In parallel, there are con- are two independent processes, which even may cepts associated with a word distributed over the entire inhibit each other” (Wernicke, 1874). cortex and connected to Wernicke’s and Broca’s areas Based on the neuropsychological method, the distinc- through the “indirect” route for understanding tion between phonological representations and nonlin- (“semantic route”) and uttering thoughts. “Soon after guistic representations of conceptual knowledge has we have learned to speak a word, we lose the intention been incorporated in most modern (Dell, Martin, & only to reproduce sounds and plan to utter a meaning” Schwartz, 2007; Lambon Ralph, Graham, Ellis, & (Wernicke, 1874). “We have to assume that (then) the Hodges, 1998; Levelt, 1999; Morton, 1980)aswellashis- majority of speech impulses reach the word concepts torical (Freud, 1891; Goldstein, 1927; Kleist, 1905,see from the remaining cerebral cortex” (Wernicke, 1906). Weiller, Bormann, Saur, Musso, & Rijntjes, 2011)models Here, we have the first description of a brain network of language processing. In all cognitive models of word with nodes and connections. processing, the mapping is achieved through different The ensuing confusion about the locations of associa- layers of representations, but all these models assume tion tracts for these two routes was partly due to the at least two parallel cognitive streams. insistence by Wernicke that those tracts mediating the It was Carl Wernicke (at 26 years old) who, in his processing of the “Wortbegriff” (i.e., the “direct” route) “physiological model on an anatomical basis,” devel- should be located behind the insula, and conduction oped a central and very modern idea of how language aphasia postulated as a consequence of an isolated is processed in the brain (Wernicke, 1874). Wernicke damage of this direct route was not found in insular assumed only two centers in the brain, “the center lesions (for more details see Weiller et al., 2011). Today, for images of movement for sound production in the function Wernicke ascribed to the direct route (e.g., the first frontal convolution” (i.e., the inferior frontal sensorimotor mapping) is equivalent to what we today gyrus [IFG], called Broca’s area) and “a sensory would ascribe to the dorsal route along the arcuate fas- language center, containing the storage of sound cicle/superior longitudinal fascicle. Wernicke did not images of speech in the first temporal convolution” make any differentiation between dorsal and ventral (i.e., the superior temporal gyrus [STG], later called tracts; however, he explicitly, clearly, and repeatedly Wernicke’s area), and all language functions would be mentioned the extreme capsule that is today seen as the derived from the interaction between both centers. major connection of the ventral stream. He referred to
Neurobiology of Language. DOI: http://dx.doi.org/10.1016/B978-0-12-407794-2.00027-4 325 © 2016 Elsevier Inc. All rights reserved. 326 27. THE DUAL LOOP MODEL IN LANGUAGE the notion of his academic mentor Meynert, who was system in the brain (Demonet, Thierry, & Cardebat, the first to ascribe a language function to a set of 2005; Hickok & Poeppel, 2004; Rauschecker, 1998; regions comprising the claustrum, the insula, as well as Scott, Blank, Rosen, & Wise, 2000; Wise, 2003): the the ascending acoustic fibers in the external and dorsal stream is involved in mapping speech sound to extreme capsule (Meynert, 1866). Wernicke was aware articulation, whereas the ventral one would support of other association tracts (e.g., the arcuate fascicle speech to meaning correspondences. In these models, [AF]) that he saw “not actually a special bundle, but a the frontal termination of the ventral stream has not general system of association fibers, which must be exactly been determined and Broca’s area is sometimes considered in the anatomy of speech regions” described only in the context of the dorsal stream. (Wernicke, 1906). Later, under the influence of eminent Wise (2003), favoring the anterior temporal lobe (ATL) researchers in Wernicke’s time (von Monakow, as decisive for language comprehension, pointed to the Charcot, Dejerine; see Weiller et al., 2011), the arcuate uncinate fascicle (UF) as a ventral connection, as has fascicle was established as the main or sometimes only been supported by DTI studies (Friederici, Bahlmann, connecting tract between Wernicke’s and Broca’s areas. Heim, Schubotz, & Anwander, 2006; Parker et al., Geschwind’s iconic diagram with an anterior “lan- 2005). Coming from the gold standard, tracing guage center” in the inferior frontal region, commonly experiments in monkeys, Pandya’s group suggested related to speech production, a posterior temporal the extreme capsule as an important connecting path- region, related to speech comprehension connected way in language, and also in grammar, connecting the through a single fiber system above the level of the ven- temporal lobe with what is seen as BA 45 in humans tricles, and the arcuate fascicle, along which language (Pandya & Yeterian, 1996; Petrides & Pandya, 1988, information is transferred, has been the blueprint that 2009; Petrides & Pandya, 2002, 2009; Schmahmann & almost all textbooks refer to (Geschwind, 1972). Pandya, 2006). Geschwind’s preference for the arcuate fascicle (see This was the situation when we aimed to integrate Weiller et al., 2011) may be due to the importance he functional connotations with tract morphology to test gave to the angular gyrus as multimodal integration the anatomical basis of the “dual-stream model” as it area for language: “the function of Wernicke’s area was proposed by Hickok and Poeppel (2004) by implies the existence of extensive connexions to the combining fMRI with diffusion tensor imaging (DTI), angular gyrus region” (Geschwind, 1965). Thus, the assuming a distributed network comprising special- ventral pathway along the extreme capsule was out of ized brain areas (network nodes) and their intercon- sight until recently (Weiller et al., 2011). necting white matter fiber tracts (network connections) Although the notion of a ventral pathway connect- (Saur et al., 2008). The findings revealed that a sublexi- ing temporal and frontal lobes for language processing cal, phonological speech task (pseudoword repetition) got lost, the idea of a dual stream model emerged in was sustained by a dorsal pathway connecting the the area of vision, assuming two parallel processes for superior temporal lobe and premotor cortices in perception of visual stimuli: “one ambient, determin- the frontal lobe via superior longitudinal fascicles and ing space at large around the body, the other focal, the arcuate fascicle. In contrast, a higher-level language which examines detail in small areas or space” comprehension task was mediated by a ventral path- (Trevarthen, 1968). This idea developed into the very way connecting the middle temporal lobe and the ven- well-known ventral “what” and dorsal “where/how” trolateral prefrontal cortex via the extreme capsule. pathways (Kravitz, Saleem, Baker, & Mishkin, 2011; The finding of the extreme capsule as the place for Milner & Goodale, 1995; Mishkin, Ungerleider, & connecting fibers within the ventral pathway was sup- Macko, 1983). The processing of a “where” and “what” ported by similar publications on DTI trackings in of a visual stimulus take different courses, both start- humans (Croxson et al., 2005; Frey, Campbell, Pike, & ing in the primary visual cortex but with a subdivision Petrides, 2008; Friederici et al., 2006; Makris & Pandya, in dorsal and ventral streams already present in extra- 2009; Parker et al., 2005). striate regions, extending toward the parietal and tem- Evidence from functional studies support the idea poral lobe, respectively. Over the years, a subdivision of the dual loop model; during presurgical assessment of different processing streams was also proposed in of epileptic patients, stereo-electroencephalographic the motor system (Rizzolatti & Matelli, 2003) or for recordings were performed and ERP signals were visuospatial attention (Corbetta, Kincade, Lewis, recorded during a phoneme task on a pair of pseudo- Snyder, & Sapir, 2005). Studies of comparative anat- words and a lexical-semantic task on adjective-nouns omy revealing two processing streams for the acoustic pairs. Phonological information processing predomi- modalities (Romanski et al., 1999) and a larger number nantly occurred in the left supramarginal gyrus (SMG) of imaging studies in humans led to a “new” hypothe- (dorsal stream) and processing lexicosemantic informa- sis of dual stream processing for auditory language tion occurred in the anterior/middle temporal and
D. LARGE-SCALE MODELS 27.1 PATIENTS 327 fusiform gyrus (ventral stream) (Trebuchon, Demonet, Hickok, 2009, 2012; Quigg, Geldmacher, & Elias, 2006) Chauvel, & Lie´geois-Chauvel, 2013). Stimulating the or SMG (Axer, von Keyserlingk, Berks, & von dorsal pathway with electrostimulation leads to pho- Keyserlingk, 2001; Baldo & Dronkers, 2006; Baldo, nological paraphasias (Leclercq et al., 2010), whereas Katseff, & Dronkers, 2012) lead to the syndrome of electrostimulation of the ventral EmC leads to seman- conduction aphasia. Tracts or cortical regions, both tic paraphasias (Duffau et al., 2005). constellations, evidence the dorsal stream as respon- sible for conduction aphasia. This consideration could also be taken into account 27.1 PATIENTS when trying to understand symptoms in degenerative disease. The logopenic variant of primary progressive Results from patients with acute aphasia support aphasia (PPA) has also similar symptoms as conduc- the claim that language is processed within a dual tion aphasia and is characterized by intact word com- pathway network. Repetition impairments were prehension, but it has repetition and phonological mainly associated with posterior temporoparietal impairments (Galantucci et al., 2011) and is associated regions and damage of the AF/SLF, whereas com- with atrophy of temporoparietal regions. Impaired prehension impairments were associated with lesions phonological processing can be explained by deficits in more ventrally in temporoprefrontal regions project- tasks that require phonological storage and the pres- ing on the ventral EmC (Kuemmerer et al., 2013). ence of phonological paraphasias (Gorno-Tempini Although this study complemented and supported et al., 2008). Results of studies using DTI, fractional the previous DTI study, patients commonly present anisotropy (FA), and volumetric studies (Galantucci with syndromes (i.e., a typical collection of symp- et al., 2011; Gorno-Tempini et al., 2008; Hu et al., 2010) toms). Ueno, Saito, Rogers, and Lambon Ralph (2011) demonstrate the involvement of the dorsal pathway implemented the dual pathway network in a compu- (phonological loop) and also gray matter atrophy in tational model and could virtually relate symptoms these patients, supporting the role of the dorsal stream like repetition and comprehension impairments and in phonological processing. also syndromes like Wernicke’s and Broca’s aphasia Semantic dementia may also be seen in light of the to the expected lesion sites. Allocation of symptom dual loop model. This disorder is characterized by collections to syndromes could also be related to impaired comprehension and naming, but intact repe- lesions in acute aphasic patients (Kuemmerer et al., tition (Jefferies, Patterson, Jones, & Lambon Ralph, 2012). Lesions associated with Broca’s aphasia were in 2009; Lambon Ralph et al., 1998; Mummery et al., 1999; theIFG,Insula,andSMG,whereaslesionscorrelating Wilson et al., 2009). Atrophy in these patients is with Wernicke’s aphasia were in the STG, postcentral located in the ATL/temporal lobe/ventral semantic gyrus, and Insula. Semantic paraphasias and compre- processing stream of the temporal lobe (Agosta et al., hension impairments in Wernicke’s aphasia may be 2010; Galton et al., 2001; Hodges, Patterson, Oxbury, & due to temporal lesions and damage to the ventral Funnell, 1992). Within the computational model of pathway, whereas phonemic paraphasias may be Ueno et al. (2011), the specific symptom constellation related to damage to the dorsal pathway. Thus, in patients with semantic dementia could be elicited Wernicke aphasia affects both the ventral and the by virtual damage to the ATL and anterior STG, dorsal pathway. supporting the relevance of the ventral pathway in Another aphasia syndrome, conduction aphasia semantic dementia. (Damasio & Damasio, 1980; Poncet, Habib, & Taken together, damage within the dual pathway Robillard, 1987), is characterized by fluent, meaningful model has an effect on language impairments of spontaneous speech with preserved auditory compre- patients with acute aphasia in stroke (Fridriksson et al., hension but frequent phonemic paraphasias and repe- 2010; Hosomi et al., 2009; Kuemmerer et al., 2013), as tition impairments (Bernal & Ardila, 2009; Damasio & well as on patients with chronic progressive language Damasio, 1980; Hickok, 2012; Weiller et al., 2011). The impairments, like semantic dementia or logopenic PPA original conception of conduction aphasia as a dis- (Schwindt et al., 2013). Within this model it is possible connection syndrome (Wernicke, 1874)throughdam- to relate different symptoms and syndromes to differ- age to the AF/SLF (Geschwind, 1965) is supported by ent lesion sites. However, most cognitive processes do several recent studies (Duffau, Peggy Gatignol, naturally require an interaction of both pathways Mandonnet, Capelle, & Taillandier, 2008; Yamada (Ueno et al., 2011; Weiller et al., 2011). Therefore, it is et al., 2007). However, many other contemporary essential to further explore how different models of studies favor the idea that lesions to cortical gray mat- connectivity relate to language impairments to improve ter in the left inferior parietal and superior temporal our understanding of the functional relevance of both lobe (Anderson et al., 1999; Bartha & Benke, 2003; pathways (Dick & Tremblay, 2012).
D. LARGE-SCALE MODELS 328 27. THE DUAL LOOP MODEL IN LANGUAGE
27.2 NEUROSPSYCHOLOGY individual we worked with was asked to repeat the words “czar” and “raw” on two different occasions. We have seen that patient studies have played an She produced “castle” and “meat” instead. This important role in the development of early models of syndrome suggests a severe impairment to the phono- language processing in the brain. The approach of logical loop and reliance on semantic information Wernicke, Lichtheim, and others, however, eventually derived from the auditorily presented word. However, grew out of fashion, partially because predictions the semantic errors in repetition suggest the additional about the localization of cognitive functions proved to involvement of a mild semantic impairment in this be wrong (Head, 1926). In a revival of this type of syndrome besides the severe impairment in the non- approach beginning in the 1970s, cognitive neuropsy- lexical repetition route. A similar, yet milder, deficit is chology has been most influential in developing cogni- present in another syndrome, impaired phonological tive models of language processing (Shallice, 1988; short-term memory (STM). This is sometimes also Rapp, 2001). Early research in acquired dyslexia has referred to as repetition conduction aphasia (Shallice & led to the proposal of a dual-route model of reading Warrington, 1977). These patients also suffer from based on dissociations among dyslexic individuals reduced spans for digits and words and impaired rep- (Coltheart, Patterson, & Marshall, 1980). One route, the etition of long nonwords. Processing the meaning of lexical-semantic route, involved mapping of the visual stimuli presented for repetition is better preserved. In word onto a semantic representation and subsequent sentence repetition, STM patients appear to have the access of the phonological word form in the mental meaning of the sentence preserved, suggesting lexicon. The other route, the so-called sublexical route, involvement of semantic processing in this task (Baldo, involved the mapping of graphemes onto their respec- Klostermann, & Dronkers, 2008). It has been argued tive sounds without access to the word’s representa- that deep dysphasia and STM deficit reflect the contin- tion in the mental lexicon. Evidence for this dual-route uum of a deficit rather than two independent model came from patients with phonological dyslexia syndromes (Martin, Saffran, & Dell, 1996). who were unable to use their sublexical route: They Cognitive neuropsychology has preferably used are unable to read nonwords but are able to read this type of dissociation among tasks to develop regular and exception words. Please note that the models of complex cognitive skills. More recently, “dual-route” in reading may not be identical with however, associations of functional impairments have the proposed anatomical dual-route system along the been used to develop models further. In a recent AF/SLF and extreme capsule tracts. study, Dell, Schwartz, Nozari, Faseyitan, and Coslett The mirror impairment, surface dyslexia, can be (2013) have mapped the parameters of a dual-route observed in patients with a semantic impairment and model of naming and repetition onto neural regions. is characterized by a predominant reliance on the sub- Their model is a dual-route interactive model, which lexical reading route. Comparable dissociations and has been implemented as a computer model. In this “syndromes” have also been reported for repetition, model, a representation of a phonological input is suggesting the involvement of at least two routes in interactively linked to phonological output units, a this task. McCarthy and Warrington (1984) reported lexical and a semantic layer. The connections between three individuals, two with conduction aphasia and the input and the phonological output units represent one with transcortical motor aphasia. The authors the nonlexical, nonsemantic route. In contrast, during argued that two routes were involved in repetition and repetition of single words, lexical and semantic repre- speech production: a fast, automatic phonological sentations are activated in parallel, reflecting the con- route and a slow semantic route. McCarthy and tribution of a word’s lexical status and its meaning. Warrington (2001) reported a patient with a severe The model has been successfully “fitted” to large semantic impairment due to semantic dementia. The groups of aphasic individuals. With some exceptions, patient had a severe naming impairment and was also an aphasic person’s pattern in naming and repetition considerably impaired in word comprehension tasks. can be simulated by changing parameters in the However, his digit span was preserved. A different computer model (Dell et al., 2007). This means that the syndrome is deep dysphasia, which consists of a pattern of errors of an aphasic speaker can be simu- severe repetition deficit. Patients with deep dysphasia lated within that model, and each aphasic participant are rare but present with an impressive, counterintui- is represented by a specific combination of model tive pattern of strengths and weaknesses. They usually parameters. have a severely limited digit span, not exceeding a In their more recent study, Dell et al. (2013) single digit. They are unable to repeat nonwords, and mapped the individual patients’ model parameters they produce semantic errors in repetition tasks. One onto lesions. Artificial lesions to the lexical-semantic
D. LARGE-SCALE MODELS 27.4 ANATOMY, HUBS, DIVISIONS 329 connections in the computer model were correlated and “internal models or emulators” (Rauschecker & with neural lesions in anterior temporal areas, inferior Scott, 2009). Thus, the dorsal stream is responsible for temporal areas, IFG, and the SMG. These regions had the ordering of elements in a continuous string to been identified as substrates of various aspects of pro- assure a correct production of behavior (e.g., subse- cessing of meaning in the brain. In contrast, artificial quent syllables, word order, movement trajectories, lesions to the phonological output representations in orienting to a visual stimulus, and updating the place the computer model mapped onto the SMG, postcen- value of an Arab digit), irrespective of whether this tral gyrus, precentral gyrus, and insula what the behavior has been executed before or has a meaning. authors suggest is the “anterior part of the dorsal Therefore, processing is “time-dependent.” In lan- stream.” The model’s connections between auditory guage, correct phonology may be learned through imi- input and output phonemes mapped onto “the STG, tation and repetition, and the dorsal stream may serve the posterior third of the planum temporale and as an automated correction mechanism for correct pro- cortex at the juncture of the parietal and temporal duction of speech. This function is typically attributed lobes (area Spt) as well as the SMG and postcentral to what is called the dorso-dorsal stream (along SLF II) gyrus” (Dell et al., 2013). (Binkofski & Buxbaum, 2013; Hoeren et al., 2014; Vry et al., 2012; Vry et al., 2014), which connects with dor- sal premotor cortex. Through exercise and experience, 27.3 FUNCTIONS OF THE DUAL LOOP the sequences can be converted into blueprints (e.g., MODEL one’s own signature; Rijntjes et al., 1999) that are stored in SMG and BA 44 in IFG (“canonical neurons”) There is no reason to suppose that the organization and may relate to context and semantics, thus acces- of the acoustic language system is different from other sing areas in the inferior parietal cortex (IPC) and pos- modalities. Thus, a dual loop system has been postu- terior temporal lobe, constituting what is called the lated in various domains (see Rijntjes, Weiller, dorsal-ventral stream (SLF III and arcuate fascicle) Bormann, & Musso, 2012 for an overview of various (Binkofski & Buxbaum, 2013; Hoeren et al., 2014; Vry studies showing an involvement of a dorsal and a ven- et al., 2014). Recall and execution of stored blueprints tral pathway). Thus, the function ascribed to dorsal or might be possible rapidly and without the dorso- ventral pathways in each modality may differ, but dorsal stream, and thus may substitute, in part, the only in their modality-specific aspect (Rijntjes et al., work of the dorso-dorsal stream. Adaptations in the 2012). Discussions have taken place regarding how the blueprints (e.g., changing to a new swing of a golf-pro) common aspects of processing in the dorsal and ven- may require temporary relearning through the dorso- tral streams in different modalities might be described dorsal stream. (Hickok & Poeppel, 2007; Rauschecker & Scott, 2009; Most scientists would agree that the ventral stream is Rijntjes et al., 2012; Weiller et al., 2011; Weiller, Musso, involved in meaning. We postulated that, in more Rijntjes, & Saur, 2009). general terms, the ventral pathway would be involved We postulated that a dual loop system, comprising in the identification of the structural (hierarchical) rela- long association tracts connecting prerolandic and tions of elements that may not be adjacent, and thus postrolandic parts of the brain with different computa- “time-independent,” independent of the sequence of tional abilities, provides a scaffolding system around occurrence (Weiller et al., 2011), as in grammar which various functions may have been developed (Friederici et al., 2006; Rauschecker & Scott, 2009; Weiller (Rijntjes et al., 2012; Weiller et al., 2011). It may be the et al., 2009), in tonal dependencies in music or in the cat- synergy between time-sensitive analysis of sequences egorical identification of the digits involved in difficult comparing the (correct) serial alignment of segments mental arithmetic (Klein, Korbinian, Glauche, Weiller, & with acquired (e.g., phonological) representations as a Willmes, 2012)(Willmes, Korbinian, & Klein, 2014). Also possible function of the dorsal stream and identifica- in the visuospatial domain, relevance and meaning of tion of an invariant set of auditory (and probably also stimuli require the ventral stream (Umarova et al., 2010) visual) hierarchical structural relationships between as well as imagery of movement (Vry et al., 2012)or the elements (e.g., words), that is, time-independent, pantomiming (Hoeren et al., 2014; Vry et al., 2014). along the ventral stream, which makes language possi- ble (Weiller et al., 2011). The dorsal stream is not limited to “where” or 27.4 ANATOMY, HUBS, DIVISIONS “how” functions; rather, it analyzes the sequence of elements in time and in space, allowing for a fast A clear distinction should be made between the terms online integration between sensory event information “streams” and “tracts.” Processing “streams” address
D. LARGE-SCALE MODELS 330 27. THE DUAL LOOP MODEL IN LANGUAGE the functions that are thought to be mediated by the ven- ventral pathway comprises fibers running through the tral or dorsal pathways, which include tracts and the extreme capsule (Makris & Pandya, 2009) and the UF. cortical regions connected by them. The term “tracts” Fibers in the ventral part of the external and extreme should be reserved for the anatomical correlates (here, of capsule have similar orientations and contribute to what long association tracts) connecting these cortical regions. in humans is called the IFOF (inferior frontal-occipital Tracts themselves do not have functions; they only fasciculus) (Axer, Klingner, & Prescher, 2013; Ferna´ndez- mediate between cortical areas, and the result of this Miranda, Rhoton, Kakizawa, Choi, & Alvarez-Linera, interaction might lead to a constellation that we recog- 2008; Gierhan, 2013). Thus, fibers from different cortical nize as a “function” or, in the clinical setting, a symptom areas join and leave the IFOF, not only in the frontal or may be attributed to its disturbance. We know that occipital lobes (as suggested by its name) but also in the inside one stream several tracts are known to connect temporal and parietal lobes (Umarova et al., 2010), which different brain areas, and because we also know that cer- is not unlike entering and exiting a highway. The UF can tain types of functional processing take place in this be differentiated from the fibers of the extreme capsule stream, we may equate one cortico-cortical connection and mainly connects medial and anterior temporal lobe with one of these functions. But we have to be careful regions with inferior frontal cortex. It is unclear whether here. As stated elsewhere, “Interruption of the network there are direct ventral connections between inferior has an impact on the remaining (“intact”) parts of the parietal lobule and prefrontal cortex, as suggested by network. In other words, the functions of Broca’s or human studies (Caspers et al., 2011; Catani, Howard, Wernicke’s area with an intact arcuate fascicle may not Pajevic, & Jones, 2002; Umarova et al., 2010; Vry et al., be the same as after that fascicle’s destruction.” And “... 2012) but without clear proof in primate studies the destruction of the interconnection (of the arcuate fas- (Schmahmann & Pandya, 2006). A connection between cicle) may not result in a solitary repetition failure, but IPC and the temporal lobe was seen in primates studies; in a complete new phenomenological constellation, as the middle longitudinal fascicle (mdlF) (Seltzer & the tract lesion affects the function of the regions it con- Pandya, 1984) has been found in humans (Makris & nects, and other regions in the remaining network, Pandya, 2009; Saur et al., 2008; Wong, Chandrasekaran, including in the other hemisphere, may become opera- Garibaldi, & Wong, 2011), but stimulation studies have tional” (Rijntjes et al., 2012). However, this does not con- not confirmed this connection so far (DeWitt Hamer, tradict the assumption that a particular connection in a Morit-Gasser, Gatignol, & Duffau, 2011). network on its own is necessary for a specific function The exact anatomy of the fiber tracts and the cortical (e.g., repetition), as was shown recently (Kuemmerer regions they connect, mainly based on tracing studies et al., 2013). in nonhuman primates as well as a discussion on the Anatomically, the segregation between dorsal and pro and cons of human DTI-based fiber tracking in ventral systems is alluded to by the orientation—in humans, are described elsewhere (Dick & Tremblay, humans superior or inferior—of the involved cortical 2012; Weiller et al., 2011)(Figure 27.1). regions (e.g., in the motor system) (Rizzolatti & Matelli, Conceptually, the dual loop model comprises at 2003) or in the visuospatial attention system (Corbetta least three parallel layers. As the innermost layer, func- et al., 2005). Here, we take a different approach by tionally close to the environmental end of the defining dorsal and ventral systems by the course of action perception cycle, the dorsal streams use tracts the long association tracts connecting postrolandic and to connect superior temporal lobe and IPC with pre- prerolandic brain regions, either above (i.e., “dorsal”) motor or posterior prefrontal cortex (BA 6,44, 45 B) or below (i.e., “ventral”) the sylvian fissure. Note that (Bernal & Ardila, 2009; Parker et al., 2005; Saur et al., this may give different results because cortical areas 2008, 2010). The next outer shell is provided by the may have dorsal as well as ventral connections, and ventral stream, which connects the middle and inferior thus may serve as integration hubs. temporal lobe with prefrontal cortices (BA 45A, 47) It is common ground that dorsal and ventral streams (Parker et al., 2005; Saur et al., 2008). Finally, prefrontal use various anatomical tracts. The dorsal stream uses the cortex (BA 47) and anterior temporal pole (ATL), func- superior longitudinal fascicles (SLF II, III) for parieto- tionally related to abstract and conceptual processing frontal connections and the arcuate fascicle (AF) for (Shallice & Cooper, 2013), are connected via the UF temporo-frontal connections. Depending on the frontal and may reflect the outermost layer. Also, in the parie- endings, an anatomical correlate to the functional divi- tal cortex, an onion bulb like contribution to dorsal sion originating from studies in the motor system and ventral tracts has been suggested (Caspers et al., [i.e., dorso-dorsal to premotor cortex and dorso-ventral 2011)(Figures 27.2 and 27.3). connections to prefrontal cortex (Binkofski & Buxbaum, IFG is a region within the dual loop model that has 2013)] starts to emerge (Hoeren et al., 2013, 2014). The direct ventral and dorsal connections with the two
D. LARGE-SCALE MODELS 27.4 ANATOMY, HUBS, DIVISIONS 331
integration of dorsal and ventral processing streams within Broca’s area (Musso et al., 2003; Petrides & Pandya, 2002; Thompson-Schill, D’Esposito, Aguirre, & Farah, 1997; Weiller et al., 2009). There is a consensus that syntax, generally defined as a rule system capable of generating infinite sets of sequences, may not be processed by a single, monolithic cognitive computa- tion, and thus may not be segregable in a single spe- cific, isolated brain area, but rather it is processed in a widespread network. However, opinions are contrast- ing on how many and which pathways are involved in syntax processing, which tract is more relevant for lan- guage syntax, and what kind of functional processing may underlie syntactic-related pathways. There is an argument that the arcuate fascicle, especially the part connecting with BA 44, is essential or even specific for syntax (in the context of language) and decisive for child development and evolution of humans. We sug- FIGURE 27.1 A schematic drawing of streams and tracts in the gest that dorsal and ventral streams are both needed dual loop model. Blue denotes participation in the dorsal pathway and red denotes participation in the ventral pathway. There are at for syntax (Weiller et al., 2009). In a DTI study, Wilson least three components within the dorsal system: the most superior et al. (2011) found reduced FA in patients with PPA in tract relates to the “dorso-dorsal-stream” for “sensorimotor map- the AF as well as in the ventral tracts (UF and EmC). ping” and may be mediated in humans by SLF II. The “dorso- However, a correlation between severity of syntactic ventral-stream” connects IPC with IFG along the SLF III. These two deficits and microstructural damage was related only stream connotations are derived from the motor system. The AF con- nects the temporal lobe with Pmd and IFG, probably contributing to with a decrease in FA in the arcuate within the AF/ dorso-dorsal and dorso-ventral streams. The ventral stream has at SLF tract, supporting the importance of the AF for syn- least two components, the UF connecting the anterior part of the tax. These findings do not exclude the relevance of the temporal lobe with the most inferior part of the IFG (BA 47). Fibers ventral system for syntactic processing per se; instead, that may be related to the IFOF run through the extreme capsule and they show that interruption of AF fibers is critical in connect the middle and posterior parts of the temporal lobe with inferior anterior IFG (BA 45, 47). In this diagram we give the mdLF, the breakdown of syntactic processing in this syn- which connects the temporal lobe with IPC a green color, thus attrib- drome. Studies using healthy volunteers showed that uting it neither to the dorsal nor to the ventral stream exclusively. syntax processing requires both ventral and dorsal Note that there are other opinions. Parietotemporal connections have tracts (Flo¨el, de Vries, Scholz, Breitenstein, & Johansen- been attributed to (an indirect part of) the arcuate fascicle (Catani Berg, 2009; Friederici et al., 2006; Lopez-Barroso et al., et al., 2005), and direct connections between IPC and prefrontal cortex have been postulated. Clearly, this diagram is not comprehen- 2011). In the study by Friederici et al. (2006), proces- sive for the tracts involved in language processing (e.g., tracts sing of stimuli, generated by either a finite state or a connecting to SMA or to visual association cortex as Wernicke’s per- phrase structure grammar (FSG versus PSG), was pendicular tract have been left out) but capitalizes on the dual loop linked to the ventral route. Only stimuli generated by system of long association tracts connecting prerolandic and postro- PSG were processed in the left pars opercularis of the landic parts of the brain. IFG and thus belonged to the dorsal stream, which is in line, to some extent, with the Wilson et al. (2011) data. Thus, the studies of Wilson and Friederici appear others lobes, temporal and parietal, which in turn to link the dorsal language route to syntactic complex- might act in a kind of division of labor (Plaut et al., ity. Flo¨el et al. (2009) showed that FSG is also pro- 1996) mediated by the mdLF, belonging to neither cessed in the pars opercularis and the integrity of both dorsal nor ventral streams, to master the extensive ventral and dorsal tracts predicted high performance sensory processing (e.g., AG and pMTG may both play of grammar acquisition. In stroke patients, syntax was a role in “semantic control” (Noonan et al., 2013). IFG related to both the AF and the EmC systems (Griffiths, is also the only frontal area with connections to almost Marslen-Wilson, Stamatakis, & Tyler, 2012; Rolheiser, the entire rest of the prefrontal cortex, putting it in an Stamatakis, & Tyler, 2011) and damage to the left ATL ideal situation to integrate dorsal and ventral streams predicts impairment of complex syntax processing under frontal control. This was the reason we suggest (Magnusdottir et al., 2013). Why should syntactic that syntax, essentially to extract hierarchical relation- deficits in aphasia patients, but not in PPA patients, ships out of a sequence of elements, may rely on the involve the ventral route? Etiology, disease course,
D. LARGE-SCALE MODELS 332 27. THE DUAL LOOP MODEL IN LANGUAGE
Action–perception
Insula Spt RSN 47 45 44 PmD M1 A1 STG MTG SMG AG
RSN OP4
ATL Insula
Domain independent conceptual thought
FIGURE 27.2 A diagram of connected regions of the dual loop model. Several dorsal (blue) tracts (see Figure 27.1) and ventral (red) tracts connect prerolandic (left) and postrolandic (right) brain regions. Most regions are connected by both dorsal and ventral tracts, resulting in a fully developed parallel dual loop system with reciprocal connections and equivalent pathways. Hierarchy is not determined by one specific pathway, although specific functions may primarily or crucially involve one or both, but rather by an extension of this system to regulatory, cytoarchitectonically more developed areas in prefrontal, temporal, and parietal neocortex in humans (Weiller et al., 2011). There are also regions that belong to either dorsal or ventral streams only (ATL). An onion-like structure is suggested by the different layers. For Op4, see Sepulcre (2013). RSN denotes resting-state network.
Action–perception FIGURE 27.3 Hypothetical lesion sites of various forms of language dis- orders are put on the diagram in Figure 27.2, illustrating how symp- toms or syndromes of patients might be fitted anatomically into the context Apraxia of Surface information, of the dual loop model (“work in logopenic variant, Syntax speech conduction Aphasia progress”). Broca aphasia InsulaX XSpt RSN 47 45 44 PmD M1 A1 STG MTG SMG AG RSN X OP4 X Wernicke Aphasia ATLX Insula
Semantic dementia
Domain independent conceptual thought
D. LARGE-SCALE MODELS 27.5 DEVELOPMENT 333 and functional reorganization of these two pathologies constituting a loop (Weiller et al., 2011). Figure 27.3 (aphasia and PPA) are different (Saur et al., 2006; Wilson potentially relates alterations of language to the dual et al., 2010). In PPA patients, progressive brain degenera- loop model tion correlates with decreasing and, to some extent, abnormal brain plasticity (Wilson et al., 2010). Aphasia is due to an acute event that is followed by brain reorga- 27.5 DEVELOPMENT nization. Here, brain reorganization correlates with progressive recovery of language impairments in the A recent article shows that at birth, anterior acute, subacute, and chronic states (Weiller et al., 1995; and posterior language zones can be activated specifi- Saur et al., 2006). There are also methodological differ- cally but are not yet fully functionally connected ences between the studies. The extreme capsule mask (Perani et al., 2011), and that the interaction between used for extraction of FA values and used in the more the two regions becomes significantly synchronized at recent DTI studies (Griffiths et al., 2012; Rolheiser et al., approximately 7 years of age (Friederici, Brauer, & 2011) was centered on the left IFG (BA 45), whereas Lohmann, 2011). This finding was considered in Wilson et al. (2011) used a mask starting in the insula. relation to the fact that, in contrast to the ventral Different attributions to ventral or dorsal streams may pathway, the dorsal pathway has not yet fully follow these differences. matured (Brauer, Anwander, & Friederici, 2011; There are also claims of fundamentally different Brauer, Anwander, & Friederici, 2013) and that chil- computational capacities of the various dorsal tracts, dren up to the age of 7 are rather poor at compre- with (within the language domain) a specific role for hending syntactically complex sentences (Dittmar, syntax for the tract to IFG and a clear differentiation Abbot-Smith, Lieven, & Tomasello, 2008; Dubois for language production for the other stream et al., 2008; Hahne, Eckstein, & Friederici, 2004). (Friederici et al., 2012) or a differentiation in one for Also, the full development of inner speech appears sensorimotor integration and one for phonological to occur around this age. According to Vygotsky, we processing (Catani,Jones,&ffytche,2005). In the con- do have conceptual awareness at birth, but no inner text of this chapter, similar differentiations have been speech (Vygotzky, 1934). Young children approxi- made in other domains, such as with a dorsal-dorsal mately 4 years of age accompany their actions with (for correct movement execution) and a dorsal- speech in social situations. This speech is under the ventral (for the use of blueprints) stream in the motor influence of continuous feedback from the environ- system (Hoeren et al., 2013, 2014). We advocate that ment and evolves from speech for others to overt both dorsal streams have the capacity for time- speech for oneself, called “egocentric” or “private” dependent analysis (Rauschecker & Scott, 2009), speech that is still used in social situations, but its which may be used for various functions. Also, the meaning is gradually directed at the child itself. role of working memory or the phonological loop During the process of a few years, until the age of commonly attributed to the dorsal stream (to BA 44) approximately 7 years, egocentric speech is replaced (Paulesu, Frith, & Frackowiak, 1993)inmastering by inner speech completely (Ehrich, 2006; Vygotzky, complex grammar should be taken into account. 1934). Syntactic relations, whether adjacent or long-distance, It was suggested that it is only after the internaliza- require strategies that not only are dependent on the tion of speech and after complete interaction of both temporal or spatial sequence of elements but also are pathways within the dual loop model that it is possible optimized to test a limited number of possible combi- to simultaneously combine phonological and abstract nations to convey meaningful relations. We attribute thought proficiently (Figure 27.4). One assumption is the latter features of syntax to the ventral route. One that the development of inner speech is related to the aspect, however, seems clear when looking at the cur- mastering of complex grammar, which (until the age rent literature: syntax is served by both dorsal and of 7) is something children fail in complex tasks ventral long association routes, which work in con- because of metalinguistic demands. However, for both cert, albeit with different functional specializations. hypotheses the explanation could be that, for master- A clear division of the dorsal and ventral processing ing these tasks, simultaneous analysis of both time- stream is artificial, resulting from experimental situa- dependent and time-independent processing is tions that do not reflect processing within the natural required. Only then can we start using language as a environment. For most functions, both streams would tool to represent abstract concepts (Deutscher, 2005) not be mutually exclusive but instead work in and, as Jackendoff noted, use language as a “scaffolding parallel (Cloutman, 2013; Makris & Pandya, 2009; that makes possible certain varieties of reasoning more Rauschecker & Scott, 2009; Rolheiser et al., 2011), complex than are available to nonlinguistic organisms”
D. LARGE-SCALE MODELS 334 27. THE DUAL LOOP MODEL IN LANGUAGE
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