Broca and Wernicke are dead, or moving past the classic model of language neurobiology

With the advancement of cognitive neuroscience and neuropsychological research, the field of language neurobiology is at a cross-roads with respect to its framing theories. The central thesis of this article is that the major historical framing model, the Classic "Wernicke-Lichtheim-Geschwind" model, and associated terminology, is no longer adequate for contemporary investigations into the neurobiology of language. We argue that the Classic model (1) is based on an outdated brain anatomy; (2) does not adequately represent the distributed connectivity relevant for language, (3) offers a modular and "language centric" perspective, and (4) focuses on cortical structures, for the most part leaving out subcortical regions and relevant connections. To make our case, we discuss the issue of anatomical specificity with a focus on the contemporary usage of the terms "Broca's and Wernicke's area", including results of a survey that was conducted within the language neurobiology community. We demonstrate that there is no consistent anatomical definition of "Broca's and Wernicke's Areas", and propose to replace these terms with more precise anatomical definitions. We illustrate the distributed nature of the language connectome, which extends far beyond the single-pathway notion of arcuate fasciculus connectivity established in Geschwind's version of the Classic Model. By illustrating the definitional confusion surrounding "Broca's and Wernicke's areas", and by illustrating the difficulty integrating the emerging literature on perisylvian white matter connectivity into this model, we hope to expose the limits of the model, argue for its obsolescence, and suggest a path forward in defining a replacement.

[1]  G. Hickok,et al.  Multiregional Cell Assemblies, Temporal Binding and the Representation of Conceptual Knowledge in Cortex: a Modern Theory by a “Classical” Neurologist, Carl Wernicke , 2005, Cortex.

[2]  N. Geschwind,et al.  Disconnexion Syndromes in Animals and Man: Part I , 2010, Neuropsychology Review.

[3]  A. Remhof,et al.  Towards a new , 1997 .

[4]  Costanza Papagno,et al.  What is the Role of the Uncinate Fasciculus , 2010 .

[5]  Volkmar Glauche,et al.  Ventral and dorsal pathways for language , 2008, Proceedings of the National Academy of Sciences.

[6]  Adam O. Hebb,et al.  The thalamus and language revisited , 2013, Brain and Language.

[7]  Gregory Hickok,et al.  The functional neuroanatomy of language. , 2009, Physics of life reviews.

[8]  A. Turken,et al.  The Neural Architecture of the Language Comprehension Network: Converging Evidence from Lesion and Connectivity Analyses , 2011, Front. Syst. Neurosci..

[9]  John R. Searle,et al.  The Rediscovery of the Mind , 1995, Artif. Intell..

[10]  Y. Grodzinsky,et al.  The battle for Broca’s region , 2008, Trends in Cognitive Sciences.

[11]  D. Poeppel,et al.  Towards a functional neuroanatomy of speech perception , 2000, Trends in Cognitive Sciences.

[12]  Pascale Tremblay,et al.  Beyond the arcuate fasciculus: consensus and controversy in the connectional anatomy of language. , 2012, Brain : a journal of neurology.

[13]  Tianzi Jiang,et al.  Determination of the posterior boundary of Wernicke's area based on multimodal connectivity profiles , 2015, Human brain mapping.

[14]  Emmanuel A Stamatakis,et al.  Functional organization of the neural language system: dorsal and ventral pathways are critical for syntax. , 2013, Cerebral cortex.

[15]  S H Greenblatt,et al.  Alexia without agraphia or hemianopsia. Anatomical analysis of an autopsied case. , 1973, Brain : a journal of neurology.

[16]  H. Lissauer,et al.  A case of visual agnosia with a contribution to theory , 1988 .

[17]  Cornelius Weiller,et al.  How the ventral pathway got lost – And what its recovery might mean , 2011, Brain and Language.

[18]  Sarah M. E. Gierhan Connections for auditory language in the human brain , 2013, Brain and Language.

[19]  E. Cabanis,et al.  Paul Broca's historic cases: high resolution MR imaging of the brains of Leborgne and Lelong. , 2007, Brain : a journal of neurology.

[20]  Peter Hagoort,et al.  MUC (Memory, Unification, Control) and beyond , 2013, Front. Psychol..

[21]  Peter Hagoort,et al.  Beyond the sentence given , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[22]  Andreas Prescher,et al.  Fiber anatomy of dorsal and ventral language streams , 2013, Brain and Language.

[23]  Pascale Tremblay,et al.  The Language Connectome , 2014, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[24]  William W. Graves,et al.  Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. , 2009, Cerebral cortex.

[25]  J. Dejerine Sémiologie des affections du système nerveux , 1915 .

[26]  M. E. Shenton,et al.  Human middle longitudinal fascicle: segregation and behavioral-clinical implications of two distinct fiber connections linking temporal pole and superior temporal gyrus with the angular gyrus or superior parietal lobule using multi-tensor tractography , 2013, Brain Imaging and Behavior.

[27]  Derek K. Jones,et al.  Perisylvian language networks of the human brain , 2005, Annals of neurology.

[28]  Emmanuel Mandonnet,et al.  A re-examination of neural basis of language processing: Proposal of a dynamic hodotopical model from data provided by brain stimulation mapping during picture naming , 2014, Brain and Language.

[29]  David Poeppel,et al.  Towards a new functional anatomy of language , 2004, Cognition.

[30]  L. Garey Brodmann's localisation in the cerebral cortex , 1999 .

[31]  D. Pandya,et al.  Parietal, temporal, and occipita projections to cortex of the superior temporal sulcus in the rhesus monkey: A retrograde tracer study , 1994, The Journal of comparative neurology.

[32]  Massimo Filippi,et al.  Disruption of structural connectivity along the dorsal and ventral language pathways in patients with nonfluent and semantic variant primary progressive aphasia: A DT MRI study and a literature review , 2013, Brain and Language.

[33]  A. Friederici,et al.  Broca's area in the human brain is involved in the selection of grammatical gender for language production: evidence from event-related functional magnetic resonance imaging , 2002, Neuroscience Letters.

[34]  Alan C. Evans,et al.  Morphology, morphometry and probability mapping of the pars opercularis of the inferior frontal gyrus: an in vivo MRI analysis , 1999, The European journal of neuroscience.

[35]  N. Geschwind The organization of language and the brain. , 1970, Science.

[36]  K Amunts,et al.  Quantitative analysis of sulci in the human cerebral cortex: Development, regional heterogeneity, gender difference, asymmetry, intersubject variability and cortical architecture , 1997, Human brain mapping.

[37]  Hugues Duffau,et al.  Mapping the connectivity underlying multimodal (verbal and non-verbal) semantic processing: A brain electrostimulation study , 2013, Neuropsychologia.

[38]  Derek K. Jones,et al.  Occipito-temporal connections in the human brain. , 2003, Brain : a journal of neurology.

[39]  M. Lewandowsky Praktische Neurologie für Ärzte , 1912 .

[40]  Commentary on Bajada et al., (2015) , 2016, Cortex.

[41]  J. Nielsen,et al.  Agnosia, apraxia, aphasia: Their value in cerebral localization , 1946 .

[42]  D. Poeppel,et al.  The cortical organization of speech processing , 2007, Nature Reviews Neuroscience.

[43]  T. Kuhn,et al.  The Structure of Scientific Revolutions. , 1964 .

[44]  H. Duffau,et al.  Evidence of a middle longitudinal fasciculus in the human brain from fiber dissection , 2013, Journal of anatomy.

[45]  Russell A. Poldrack,et al.  In praise of tedious anatomy , 2007, NeuroImage.

[46]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[47]  A. W. Toga,et al.  A myelo-architectonic method for the structural classification of cortical areas , 2004, NeuroImage.

[48]  J. Binder The Wernicke area , 2015, Neurology.

[49]  Gehirnpathologie. I. Allgemeine Einleitung. II. Localisation. III. Gehirnblutungen. IV. Verstopfung der Hirnarterien , 1898 .

[50]  C. Wernicke,et al.  The Symptom Complex of Aphasia , 1969 .

[51]  N. F. Ramsey,et al.  Unimpaired sentence comprehension after anterior temporal cortex resection , 2008, Neuropsychologia.

[52]  Katrin Amunts,et al.  Architecture and organizational principles of Broca's region , 2012, Trends in Cognitive Sciences.

[53]  B. Wandell,et al.  The vertical occipital fasciculus: A century of controversy resolved by in vivo measurements , 2014, Proceedings of the National Academy of Sciences.

[54]  S. Pinker,et al.  The faculty of language: what's special about it? , 2005, Cognition.

[55]  A. Benton,et al.  On Aphasia , 1874, British medical journal.

[56]  Pascale Tremblay,et al.  Fiber tracking of the frontal aslant tract and subcomponents of the arcuate fasciculus in 5–8-year-olds: Relation to speech and language function , 2015, Brain and Language.

[57]  Ernst. Scharrer Vom Bau und Leben des Gehirns , 1936 .

[58]  M. Catani,et al.  A novel frontal pathway underlies verbal fluency in primary progressive aphasia. , 2013, Brain : a journal of neurology.

[59]  Costanza Papagno,et al.  What is the role of the uncinate fasciculus? Surgical removal and proper name retrieval. , 2011, Brain : a journal of neurology.

[60]  Gregory Hickok,et al.  The architecture of speech production and the role of the phoneme in speech processing , 2014, Language and cognitive processes.

[61]  D. Poeppel,et al.  Dorsal and ventral streams: a framework for understanding aspects of the functional anatomy of language , 2004, Cognition.

[62]  I. Olson,et al.  Dissecting the uncinate fasciculus: disorders, controversies and a hypothesis. , 2013, Brain : a journal of neurology.

[63]  Catherine J. Stoodley,et al.  Consensus Paper: Language and the Cerebellum: an Ongoing Enigma , 2013, The Cerebellum.

[64]  G. Smith,et al.  Die Cytoarchitektonik der Hirnrinde des erwachsenen Menschen. , 1927 .

[65]  P. Caffarra,et al.  Alexia without agraphia or hemianopia. , 1987, European neurology.

[66]  A. Ardila,et al.  [The language area of the brain: a functional reassessment]. , 2016, Revista de neurologia.

[67]  David Poeppel,et al.  Towards a New Neurobiology of Language , 2012, The Journal of Neuroscience.

[68]  B. Mazoyer,et al.  A Common Language Network for Comprehension and Production: A Contribution to the Definition of Language Epicenters with PET , 2000, NeuroImage.

[69]  F. Guenther Cortical interactions underlying the production of speech sounds. , 2006, Journal of communication disorders.

[70]  Cornelius Weiller,et al.  Revisiting the Functional Specialization of Left Inferior Frontal Gyrus in Phonological and Semantic Fluency: The Crucial Role of Task Demands and Individual Ability , 2013, The Journal of Neuroscience.

[71]  Fang-Cheng Yeh,et al.  Rethinking the role of the middle longitudinal fascicle in language and auditory pathways. , 2013, Cerebral cortex.

[72]  Jelliffe Vergleichende Lokalisationslehre der Grosshirnrinde , 1910 .

[73]  Angela D. Friederici,et al.  The language skeleton after dissecting meaning: A functional segregation within Broca's Area , 2015, NeuroImage.

[74]  Lorraine K. Tyler,et al.  Dynamic Processing in the Human Language System: Synergy between the Arcuate Fascicle and Extreme Capsule , 2011, The Journal of Neuroscience.

[75]  P. Hagoort Nodes and networks in the neural architecture for language: Broca's region and beyond , 2014, Current Opinion in Neurobiology.

[76]  C. Price The anatomy of language: a review of 100 fMRI studies published in 2009 , 2010, Annals of the New York Academy of Sciences.

[77]  J. Rauschecker,et al.  Maps and streams in the auditory cortex: nonhuman primates illuminate human speech processing , 2009, Nature Neuroscience.

[78]  Paul M. Thompson,et al.  What is where and why it is important , 2007, NeuroImage.

[79]  Elizabeth A. Hirshorn,et al.  Localizing interference during naming: Convergent neuroimaging and neuropsychological evidence for the function of Broca's area , 2009, Proceedings of the National Academy of Sciences.

[80]  Angela D. Friederici,et al.  An fMRI study dissociating distance measures computed by Broca's area in movement processing: clause boundary vs. identity , 2015, Front. Psychol..

[81]  Edward Sapir,et al.  Language: An Introduction to the Study of Speech , 1955 .

[82]  N. Dronkers,et al.  Lesion analysis of the brain areas involved in language comprehension , 2004, Cognition.

[83]  Daniel Casasanto,et al.  Music and Language Syntax Interact in Broca’s Area: An fMRI Study , 2015, PloS one.

[84]  C. Wernicke,et al.  Lehrbuch der Gehirnkrankheiten für Aerzte und Studirende , 1881 .

[85]  Brian A. Wandell,et al.  Anatomy of the visual word form area: Adjacent cortical circuits and long-range white matter connections , 2013, Brain and Language.

[86]  M. Lorch The merest Logomachy: The 1868 Norwich discussion of aphasia by Hughlings Jackson and Broca. , 2008, Brain : a journal of neurology.

[87]  Angela D. Friederici,et al.  The ontogeny of the cortical language network , 2016, Nature Reviews Neuroscience.

[88]  Josef P. Rauschecker,et al.  Wernicke’s area revisited: Parallel streams and word processing , 2013, Brain and Language.

[89]  C. Wernicke Der aphasische Symptomencomplex: Eine psychologische Studie auf anatomischer Basis , 1874 .

[90]  G. E. Smith A New Topographical Survey of the Human Cerebral Cortex, being an Account of the Distribution of the Anatomically Distinct Cortical Areas and their Relationship to the Cerebral Sulci. , 1907, Journal of anatomy and physiology.

[91]  C Büchel,et al.  Brain regions involved in articulation , 1999, The Lancet.

[92]  Angela D. Friederici,et al.  Grounding language processing on basic neurophysiological principles , 2015, Trends in Cognitive Sciences.

[93]  Cornelius Weiller,et al.  The dual loop model: its relation to language and other modalities , 2012, Front. Evol. Neurosci..

[94]  Peter Hagoort,et al.  The neurobiology of language beyond single-word processing , 2019, Science.

[95]  W. Penfield,et al.  Speech and Brain‐Mechanisms , 1960 .

[96]  Kiyoshi Saito,et al.  Neural Basis of Language: An Overview of An Evolving Model , 2016, Neurologia medico-chirurgica.

[97]  P. Frank,et al.  Boston Studies in the Philosophy of Science , 1968 .

[98]  Bruce Crosson,et al.  Thalamic mechanisms in language: A reconsideration based on recent findings and concepts , 2013, Brain and Language.

[99]  Frank H. Guenther,et al.  A neural network model of speech acquisition and motor equivalent speech production , 2004, Biological Cybernetics.

[100]  Mitchel S. Berger,et al.  Analysis of the subcomponents and cortical terminations of the perisylvian superior longitudinal fasciculus: a fiber dissection and DTI tractography study , 2012, Brain Structure and Function.

[101]  D. Robin,et al.  An integrative model of speech motor control: A response to Ziegler , 2003 .

[102]  D. Poeppel The neuroanatomic and neurophysiological infrastructure for speech and language , 2014, Current Opinion in Neurobiology.

[103]  Myrna F. Schwartz,et al.  What the classical aphasia categories can't do for us, and why , 1984, Brain and Language.

[104]  Cyril Poupon,et al.  Anatomical Connections of the Visual Word Form Area , 2014, The Journal of Neuroscience.

[105]  R. Graves,et al.  The legacy of the Wernicke-Lichtheim model. , 1997, Journal of the history of the neurosciences.

[106]  P. Morosan,et al.  Broca's Region: Novel Organizational Principles and Multiple Receptor Mapping , 2010, PLoS biology.

[107]  M. Wibral,et al.  Untangling cross-frequency coupling in neuroscience , 2014, Current Opinion in Neurobiology.

[108]  R. Luján Fiber Pathways of the Brain, J.D. Schmahmann, D.N. Pandya (Eds.). Oxford University Press (2006), ISBN: 0-19-510423-4 , 2008 .

[109]  S. Greenblatt,et al.  Subangular alexia without agraphia or hemianopsia , 1976, Brain and Language.

[110]  G. Bruyn Atlas of the Cerebral Sulci, M. Ono, S. Kubik, Chad D. Abernathey (Eds.). Georg Thieme Verlag, Stuttgart, New York (1990), 232, DM 298 , 1990 .

[111]  J. Trueswell,et al.  Parametric effects of syntactic–semantic conflict in Broca’s area during sentence processing , 2012, Brain and Language.

[112]  G. Hickok,et al.  Role of the left hemisphere in sign language comprehension , 2002, Brain and Language.

[113]  H. Duffau,et al.  Frontal terminations for the inferior fronto-occipital fascicle: anatomical dissection, DTI study and functional considerations on a multi-component bundle , 2011, Brain Structure and Function.

[114]  A. Campbell Histological Studies on the Localisation of Cerebral Function , 2009 .

[115]  T. Kuhn The Structure of Scientific Revolutions. Chicago (University of Chicago Press) 1962. , 1962 .

[116]  Richard J. S. Wise,et al.  Task-induced brain activity in aphasic stroke patients: what is driving recovery? , 2014, Brain : a journal of neurology.

[117]  Katrin Amunts,et al.  Segregation and Wiring in the Brain , 2012, Science.

[118]  S. Scott,et al.  The neuroanatomical and functional organization of speech perception , 2003, Trends in Neurosciences.

[119]  Rutvik H. Desai,et al.  The neurobiology of semantic memory , 2011, Trends in Cognitive Sciences.

[120]  N. Geschwind Disconnexion syndromes in animals and man. I. , 1965, Brain : a journal of neurology.

[121]  D. Pandya,et al.  The extreme capsule in humans and rethinking of the language circuitry , 2009, Brain Structure and Function.

[122]  J. Rauschecker,et al.  Neurobiological roots of language in primate audition: common computational properties , 2015, Trends in Cognitive Sciences.

[123]  J. Bogen,et al.  WERNICKE'S REGION–WHERE IS IT? , 1976, Annals of the New York Academy of Sciences.

[124]  Olaf Sporns,et al.  From simple graphs to the connectome: Networks in neuroimaging , 2012, NeuroImage.

[125]  Smith Ge,et al.  A New Topographical Survey of the Human Cerebral Cortex, being an Account of the Distribution of the Anatomically Distinct Cortical Areas and their Relationship to the Cerebral Sulci. , 1907 .

[126]  Gregory Hickok,et al.  ‘Syntactic Perturbation’ During Production Activates the Right IFG, but not Broca’s Area or the ATL , 2016, Front. Psychol..

[127]  M. L. Lambon Ralph,et al.  The anterior temporal lobe semantic hub is a part of the language neural network: selective disruption of irregular past tense verbs by rTMS. , 2010, Cerebral cortex.

[128]  M. Petrides,et al.  Orofacial somatomotor responses in the macaque monkey homologue of Broca's area , 2005, Nature.

[129]  N. Geschwind Disconnexion syndromes in animals and man. II. , 1965, Brain : a journal of neurology.

[130]  C. Westin,et al.  Human middle longitudinal fascicle: variations in patterns of anatomical connections , 2013, Brain Structure and Function.

[131]  H. Lissauer,et al.  Ein Fall von Seelenblindheit nebst einem Beitrage zur Theorie derselben , 1890, Archiv für Psychiatrie und Nervenkrankheiten.

[132]  M. Mesulam,et al.  The Wernicke conundrum and the anatomy of language comprehension in primary progressive aphasia. , 2015, Brain : a journal of neurology.

[133]  Angela D. Friederici,et al.  Linking ordering in Broca's area to storage in left temporo-parietal regions: The case of sentence processing , 2012, NeuroImage.

[134]  Claude J. Bajada,et al.  Transport for language south of the Sylvian fissure: The routes and history of the main tracts and stations in the ventral language network , 2015, Cortex.