Species-specific calls activate homologs of Broca's and Wernicke's areas in the macaque

The origin of brain mechanisms that support human language—whether these originated de novo in humans or evolved from a neural substrate that existed in a common ancestor—remains a controversial issue. Although the answer is not provided by the fossil record, it is possible to make inferences by studying living species of nonhuman primates. Here we identified neural systems associated with perceiving species-specific vocalizations in rhesus macaques using H215O positron emission tomography (PET). These vocalizations evoke distinct patterns of brain activity in homologs of the human perisylvian language areas. Rather than resulting from differences in elementary acoustic properties, this activity seems to reflect higher order auditory processing. Although parallel evolution within independent primate species is feasible, this finding suggests the possibility that the last common ancestor of macaques and humans, which lived 25–30 million years ago, possessed key neural mechanisms that were plausible candidates for exaptation during the evolution of language.

[1]  G. Rizzolatti,et al.  The Cortical Motor System , 2001, Neuron.

[2]  U. Jürgens.  Neural pathways underlying vocal control , 2002, Neuroscience & Biobehavioral Reviews.

[3]  A. Damasio,et al.  The neural basis of language. , 1984, Annual review of neuroscience.

[4]  Bruno B Averbeck,et al.  Neural representation of vocalizations in the primate ventrolateral prefrontal cortex. , 2005, Journal of neurophysiology.

[5]  Lawrence W. Barsalou,et al.  Continuity of the conceptual system across species , 2005, Trends in Cognitive Sciences.

[6]  M. Arbib,et al.  Language within our grasp , 1998, Trends in Neurosciences.

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

[8]  G. Rizzolatti,et al.  Action recognition in the premotor cortex. , 1996, Brain : a journal of neurology.

[9]  S. Wise.  Evolution of Ventral Premotor Cortex and the Primate Way of Reaching , 2007 .

[10]  H. Gouzoules,et al.  Agonistic screams differ among four species of macaques: the significance of motivation-structural rules , 2000, Animal Behaviour.

[11]  D. Pandya,et al.  Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey , 1978, Brain Research.

[12]  M. Mishkin,et al.  Species-specific calls evoke asymmetric activity in the monkey's temporal poles , 2004, Nature.

[13]  P S Goldman-Rakic,et al.  Architectonics of the parietal and temporal association cortex in the strepsirhine primate Galago compared to the anthropoid primate Macaca , 1991, The Journal of comparative neurology.

[14]  R. Seyfarth,et al.  Signalers and receivers in animal communication. , 2003, Annual review of psychology.

[15]  W. Fitch.  Vocal tract length and formant frequency dispersion correlate with body size in rhesus macaques. , 1997, The Journal of the Acoustical Society of America.

[16]  Terrence W. Deacon,et al.  The neural circuitry underlying primate calls and human language , 1989 .

[17]  Powen Ru,et al.  Multiresolution spectrotemporal analysis of complex sounds. , 2005, The Journal of the Acoustical Society of America.

[18]  G. Rizzolatti,et al.  Parietal Lobe: From Action Organization to Intention Understanding , 2005, Science.

[19]  A. Braun,et al.  Asymmetry of chimpanzee planum temporale: humanlike pattern of Wernicke's brain language area homolog. , 1998, Science.

[20]  Karl J. Friston,et al.  Hearing and saying. The functional neuro-anatomy of auditory word processing. , 1996, Brain : a journal of neurology.

[21]  David Caplan,et al.  Neurolinguistics and linguistic aphasiology , 1987 .

[22]  D. Pandya,et al.  Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey , 2002, The European journal of neuroscience.

[23]  Laurie R Santos,et al.  Primate brains in the wild: the sensory bases for social interactions , 2004, Nature Reviews Neuroscience.

[24]  A. Braun,et al.  Toward an evolutionary perspective on conceptual representation: species-specific calls activate visual and affective processing systems in the macaque. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[25]  Noam Chomsky,et al.  The faculty of language: what is it, who has it, and how did it evolve? , 2002, Science.

[26]  Richard E. Passingham,et al.  The specializations of the human neocortex , 1998 .

[27]  K. Zilles,et al.  Functional neuroanatomy of the primate isocortical motor system , 2000, Anatomy and Embryology.

[28]  Robert M. Seyfarth,et al.  Primate social cognition and the origins of language , 2005, Trends in Cognitive Sciences.

[29]  J. Hyvärinen,et al.  Functional properties of neurons in the temporo-parietal association cortex of awake monkey , 2004, Experimental Brain Research.

[30]  A. Toga,et al.  The Rhesus Monkey Brain in Stereotaxic Coordinates , 1999 .

[31]  I. Nelken,et al.  Processing of low-probability sounds by cortical neurons , 2003, Nature Neuroscience.

[32]  S. Thompson-Schill,et al.  The frontal lobes and the regulation of mental activity , 2005, Current Opinion in Neurobiology.

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

[34]  P. Strick,et al.  Imaging the premotor areas , 2001, Current Opinion in Neurobiology.

[35]  A. Braun,et al.  Auditory lexical decision, categorical perception, and FM direction discrimination differentially engage left and right auditory cortex , 2004, Neuropsychologia.

[36]  N. Geschwind,et al.  Human Brain: Left-Right Asymmetries in Temporal Speech Region , 1968, Science.

[37]  P. Goldman-Rakic,et al.  An auditory domain in primate prefrontal cortex , 2002, Nature Neuroscience.

[38]  E. T. Possing,et al.  Human temporal lobe activation by speech and nonspeech sounds. , 2000, Cerebral cortex.

[39]  D. Pandya,et al.  Architectonic parcellation of the temporal operculum in rhesus monkey and its projection pattern , 1973, Zeitschrift für Anatomie und Entwicklungsgeschichte.

[40]  J M Fischer,et al.  Cortical motor representation of the laryngeal muscles in Macaca mulatta. , 1974, Brain research.

[41]  J. Rauschecker,et al.  Processing of complex sounds in the macaque nonprimary auditory cortex. , 1995, Science.

[42]  G. Rizzolatti,et al.  Hearing Sounds, Understanding Actions: Action Representation in Mirror Neurons , 2002, Science.

[43]  Mi Sereno,et al.  Cognitive Science Society. , 2022 .

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

[45]  R. Zatorre,et al.  Voice-selective areas in human auditory cortex , 2000, Nature.

[46]  A M Galaburda,et al.  The intrinsic architectonic and connectional organization of the superior temporal region of the rhesus monkey , 1983, The Journal of comparative neurology.

[47]  Sasaki Kazuo,et al.  Cortical field potentials preceding vocalization and influences of cerebellar hemispherectomy upon them in monkeys , 1995, Brain Research.

[48]  T. Griffiths,et al.  Distinct Mechanisms for Processing Spatial Sequences and Pitch Sequences in the Human Auditory Brain , 2003, The Journal of Neuroscience.

[49]  Marc D. Hauser,et al.  The Neurophysiology of Functionally Meaningful Categories: Macaque Ventrolateral Prefrontal Cortex Plays a Critical Role in Spontaneous Categorization of Species-Specific Vocalizations , 2005, Journal of Cognitive Neuroscience.