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