The human brain is a fascinatingly complex organ with specialized structures associated with distinct functions. Classical and recent studies on brain localization propose that Broca’s area underpin expressive language and this has been generalized to explain brain functional organization. However, recent neuroimaging studies have shown that the Broca’s area is an extended network that not only participate in its primary function-expressive language processing but in secondary functions-processing non-linguistic/nonverbal tasks as well. Also, there is hierarchical connectivity and interaction of Broca’s region and different brain areas in underlying related primary functions. For this review, I start with revisiting the classical description of brain localization. I then discuss the neuroanatomy of language production and the role of Broca’s region in language processing. I then highlight the participation of the Broca’s area in non-linguistic tasks and non-primary linguistic tasks. Ultimately, I propose a novel hypothesis called integrated systems hypothesis. The integrated systems hypothesis is useful for guiding research on the multimodal role of specific localized integrated systems of the brain especially the role of the Broca’s region in integrating linguistic and non-linguistic processing and how this facilitate language production.
KeywordsBrain LocalizationBroca’s AreaBroca’s RegionIntegrated SystemIntegrated Systems Hypothesis
Finger, S. (2010) The Birth of the Localization Theory. In: Finger, S., Boller, F. and Tyler, K.L., Eds., Handbook of Clinical Neurology, Vol. 95 (3rd series) History of Neurology, 117-128.
Young, R.M (1970) Mind, Brain and Adaptation in the 19th Century. Clarendon Press, Oxford.
Finger, S. (2000) Minds behind the Brain. Oxford, New York.
Flourens, M.-J.-P. (1842) Recherches Experimentales sur les Proprie′te′s et les Fonctions du Syste`me Nerveux dans les Animaux Verte′bre′s [Experimental Research on the Properties and the Functions of the Nervous Systems in Vertebral Animals.] (2nd edn.). Baillie`re, Paris.
Flourens, M.-J.-P. (1846) Phrenology Examined (2nd Edition; de L Meigs C, trans.). Hogan and Thompson, Philadelphia.
Ardila, A., Bernal, B. and Rosselli, M. (2016) Why Broca’s Area Damage Does Not Result in Classical Broca Aphasia. Frontiers in Human Neuroscience, 10, 249. https://doi.org/10.3389/fnhum.2016.00249
Foundas, A.L., Leonard, C.M., Gilmore, R.L., Fennell, E.B. and Heilman, K.M. (1996) Pars Triangularis Asymmetry and Language Dominance. Proceedings of the National Academy of Sciences, 93, 719-722. https://doi.org/10.1073/pnas.93.2.719
Hagoort, P. (2005) Broca’s Complex as the Unification Space for Language. In: Cutler, A., Ed., Twenty-First Century Psycholinguistics: Four Cornerstones, Lawrence Erlbaum Associates, Mahwah, 157-172.
Hagoort, P. (2006) On Broca, Brain and Binding. In: Grodzinsky, Y. and Amunts, K., Eds., Broca’s Region, Oxford University Press, Oxford, 242-253. https://doi.org/10.1093/acprof:oso/9780195177640.003.0015
Lemaire, J.J., Golby, A., Wells, W.M., Pujol, S., Tie, Y., Rigolo, L., et al. (2013) Extended Broca’s Area in the Functional Connectome of Language in Adults: Combined Cortical and Subcortical Single-Subject Analysis using fMRI and DTI Tractography. Brain Topography, 26, 428-441. https://doi.org/10.1007/s10548-012-0257-7
Kadis, D.S., Dimitrijevic, A., Toro-Serey, C.A., Smith, M.L. and Holland, S.K. (2016) Characterizing Information Flux within the Distributed Pediatric Expressive Language Network: A Core Region Mapped through fMRI Constrained MEG Effective Connectivity Analyses. Brain Connect, 6, 76-83. https://doi.org/10.1089/brain.2015.0374
Bernal, B., Ardila, A. and Rosselli, M. (2015) Broca’s Area Network in Language Function: A Pooling-Data Connectivity Study. Frontiers in Psychology, 6, 687. https://doi.org/10.3389/fpsyg.2015.00687
Ardila, A., Bernal, B. and Rosselli, M. (2016b) How Localized Are Language Brain Areas? A Review of Brodmann Areas Involvement in Language. Archives of Clinical Neuropsychology, 31, 112-122. https://doi.org/10.1093/arclin/acv081
Benson, F. and Ardila, A. (1996) Aphasia: A Clinical Perspective. Oxford University Press, Oxford.
Heim, S., Eickhoff, S.B. and Amunts, K. (2008) Specialisation in Broca’s Region or Semantic, Phonological, and Syntactic Fluency? Neuroimage, 40, 1362-1368.
Kang, A.M., Constable, R.T., Gore, J.C. and Avrutin, S. (1999) An Event-Related fMRI Study of Implicit Phrase-Level Syntactic and Semantic Processing. Neuroimage, 10, 555-561. https://doi.org/10.1006/nimg.1999.0493
Grossman, M., Cooke, A., DeVita, C., Chen, W., Moore, P., Detre, J., et al. (2002) Sentence Processing Strategies in Healthy Seniors with Poor Comprehension: An fMRI Study. Brain and Language, 80, 296-313. https://doi.org/10.1006/brln.2001.2581
Sahin, N.T., Pinker, S. and Halgren, E. (2006) Abstract Grammatical Processing of Nouns and Verbs in Broca’s Area: Evidence from fMRI. Cortex, 42, 540-562.
Abrahams, S., Goldstein, L.H., Simmons, A., Brammer, M.J., Williams, S.C., et al. (2003) Functional Magnetic Resonance Imaging of Verbal Fluency and Confrontation Naming using Compressed Image Acquisition to Permit Overt Responses. Human Brain Mapping, 20, 29-40. https://doi.org/10.1002/hbm.10126
Heim, S., Eickhoff, S.B., Ischebeck, A.K., Friederici, A.D., Stephan, K.E. and Amunts, K. (2009) Effective Connectivity of the Left BA44, BA45, and Inferior Temporal Gyrus during Lexical and Phonological Decisions Identified with DCM. Human Brain Mapping, 30, 392-402. https://doi.org/10.1002/hbm.20512
Fiebach, C.J., Friederici, A.D., Müller, K. and von Cramon, D.Y. (2002) fMRI Evidence for Dual Routes to the Mental Lexicon in Visual Word Recognition. Journal of Cognitive Neuroscience, 14, 11-23. https://doi.org/10.1162/089892902317205285
Vorobyev, V.A., Alho, K., Medvedev, S.V., Pakhomov, S.V., Roudas, M.S., et al. (2004) Linguistic Processing in Visual and Modality-Nonspecific Brain Areas: PET Recordings during Selective Attention. Brain Research. Cognitive Brain Research, 20, 309-322.
Düzel, E., Picton, T.W., Cabeza, R., Yonelinas, A.P., Scheich, H., et al. (2001) Comparative Electrophysiological and Hemodynamic Measures of Neural Activation during Memory-Retrieval. Human Brain Mapping, 13, 104-123. https://doi.org/10.1002/hbm.1028
Goel, V., Gold, B., Kapur, S. and Houle, S. (1998) Neuroanatomical Correlates of Human Reasoning. Journal of Cognitive Neuroscience, 10, 293-302. https://doi.org/10.1162/089892998562744
Grodzinsky, Y. (2000) The Neurology of Syntax: Language Use without Broca’s Area. Behavioral and Brain Sciences, 23, 1-21. https://doi.org/10.1017/S0140525X00002399
Grodzinsky, Y. (2006) The Language Faculty, Broca’s Region, and the Mirror System. Cortex, 42, 464-468.
Thompson-Schill, S.L. (2005) Dissecting the Language Organ: A New Look at the Role of Broca’s Area in Language Processing. In: Cutler, A., Ed., Twenty-First Century Psycholinguistics: Four Cornerstones, Lawrence Erlbaum Associates Inc., Mahwah, 173-190.
Fadiga, L., Craighero, L., and Roy, A. (2006) Broca’s Region: A Speech Area. In Broca’s Region. In: Grodzinky, Y. and Amunts, K., Eds., Oxford University Press, New York, 137-152. https://doi.org/10.1093/acprof:oso/9780195177640.003.0009
Ardila, A. and Bernal, B. (2007) What Can Be Localized in the Brain? Towards a “Factor” Theory on Brain Organization of Cognition. International Journal of Neuroscience, 117, 935-969. https://doi.org/10.1080/00207450600912222
Novick, J.M., Trueswell, J.C. and Thompson, S.L. (2005) Cognitive Control and Parsing: Re-Examining the Role of Broca’s Area in Sentence Comprehension. Cognitive, Affective, & Behavioral Neuroscience, 5, 263-281. https://doi.org/10.3758/CABN.5.3.263
Haverkort, M. (2005) Linguistic Representation and Language Use in Aphasia. In: Cutler, A., Ed., Twenty-First Century Psycholinguistics: Four Cornerstones, Lawrence Erlbaum Associates Inc., Mahwah, 57-68.
Bookheimer, S. (2002) Functional MRI of Language: New Approaches to Understanding the Cortical Organization of Semantic Processing. Annual Review of Neuroscience, 25, 151-188. https://doi.org/10.1146/annurev.neuro.25.112701.142946
Koechlin, E. and Jubault, T. (2006) Broca’s Area and the Hierarchical Organization of Human Behavior. Neuron, 50, 963-974.
Lotze, M., Heymans, U., Birbaumer, N., Veit, R., Erb, M., Flor, H., et al. (2006) Differential Cerebral Activation during Observation of Expressive Gestures and Motor Acts. Neuropsychologia, 44, 1787-1795.
Giraud, A.L., Kell, C., Thierfelder, C., Sterzer, P., Russ, M.O., Preibisch, C., et al. (2004) Contributions of Sensory Input, Auditory Search and Verbal Comprehension to Cortical Activity during Speech Processing. Cerebral Cortex, 14, 247-255. https://doi.org/10.1093/cercor/bhg124
Zekveld, A.A., Heslenfeld, D.J., Festen, J.M. and Schoonhoven, R. (2006) Top-Down and Bottom-Up Processes in Speech Comprehension. Neuroimage, 32, 1826-1836.
Koelsch, S., Fritz, T., VCramon, D.Y., Müller, K. and Friederici, A.D. (2006) Investigating Emotion with Music: An fMRI Study. Human Brain Mapping, 27, 239-250. https://doi.org/10.1002/hbm.20180
Rama, P., Martinkauppi, S., Linnankoski, I., Koivisto, J., Aronen, H.J. and Carlson, S. (2001) Working Memory of Identification of Emotional Vocal Expressions: An fMRI Study. Neuroimage, 13, 1090-1101. https://doi.org/10.1006/nimg.2001.0777
Sun, X., Zhang, X., Chen, X., Zhang, P., Bao, M., Zhang, D., et al. (2005) Age-Dependent Brain Activation during Forward and Back Ward Digit Recall Revealed by fMRI. Neuroimage, 26, 36-47.
Rickard, T.C., Romero, S.G., Basso, G., Wharton, C., Flitman, S. and Grafman, J. (2000) The Calculating Brain: An fMRI Study. Neuropsychologia, 38, 325-335.
Yoo, S.-S., Freeman, D.K., McCarthy, J.J.III, and Jolesz, F.A. (2003) Neural Substrates of Tactile Imagery: A Functional MRI Study. Neuroreport, 14, 581-585. https://doi.org/10.1097/00001756-200303240-00011
Amunts, K., Weiss, P.H., Mohlberg, H., Pieperhoff, P., Eickhoff, S., Gurd, J.M., et al. (2004) Analysis of Neural Mechanisms Underlying Verbal Fluency in Cytoarchitectonically Defined Stereotaxicspace—The Roles of Brodmann Areas 44 and 45. Neuroimage, 22, 42-56.
Cabeza, R. and Nyberg, L. (2000) Imaging Cognition II: An Empirical Review of 275 PET and fMRI Studies. Cognitive Neuroscience, 12, 1-47. https://doi.org/10.1162/08989290051137585
D’Esposito, M., Postle, B.R., Ballard, D. and Lease, J. (1999) Maintenance versus Manipulation of Information Held in Working Memory: An Event-Related fMRI Study. Brain and Cognition, 41, 66-86. https://doi.org/10.1006/brcg.1999.1096
Amunts, K., Lenzen, M., Friederici, A.D., Schleicher, A., Morosan, P., Palomero-Gallagher, N., et al. (2010) Broca’s Region: Novel Organizational Principles and Multiple Receptor Mapping. PLOS Biology, 8, e1000489. https://doi.org/10.1371/journal.pbio.1000489
Hickok, G. and Poeppel, D. (2000) Towards a Functional Neuroanatomy of Speech Perception. Trends in Cognitive Sciences, 4, 131-138.
Hickok, G. and Poeppel, D. (2004) Dorsal and Ventral Streams: A Framework for Understanding Aspects of the Functional Anatomy of Language. Cognition, 92, 67-99.
Hickok, G. and Poeppel, D. (2007) The Cortical Organization of Speech Processing. Nature Reviews Neuroscience, 8, 393-402. https://doi.org/10.1038/nrn2113
Abrams, D.A., Ryali, S., Chen, T., Balaban, E., Levitin, D.J. and Menon, V. (2013) Multivariate Activation and Connectivity Patterns Discriminate Speech Intelligibility in Wernicke’s, Broca’s and Geschwind’s Areas. Cerebral Cortex, 23, 1703-1714. https://doi.org/10.1093/cercor/bhs165