Processing of vocalizations in humans and monkeys: A comparative fMRI study

Humans and many other animals use acoustical signals to mediate social interactions with conspecifics. The evolution of sound-based communication is still poorly understood and its neural correlates have only recently begun to be investigated. In the present study, we applied functional MRI to humans and macaque monkeys listening to identical stimuli in order to compare the cortical networks involved in the processing of vocalizations. At the first stages of auditory processing, both species showed similar fMRI activity maps within and around the lateral sulcus (the Sylvian fissure in humans). Monkeys showed remarkably similar responses to monkey calls and to human vocal sounds (speech or otherwise), mainly in the lateral sulcus and the adjacent superior temporal gyrus (STG). In contrast, a preference for human vocalizations and especially for speech was observed in the human STG and superior temporal sulcus (STS). The STS and Broca's region were especially responsive to intelligible utterances. The evolution of the language faculty in humans appears to have recruited most of the STS. It may be that in monkeys, a much simpler repertoire of vocalizations requires less involvement of this temporal territory.

[1]  Christoph Kayser,et al.  Voice Cells in the Primate Temporal Lobe , 2011, Current Biology.

[2]  D. Pandya,et al.  Architectonic analysis of the auditory‐related areas of the superior temporal region in human brain , 2007, The Journal of comparative neurology.

[3]  J B Poline,et al.  Brain imaging of language plasticity in adopted adults: can a second language replace the first? , 2001, NeuroImage.

[4]  D. V. van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex. , 2005, NeuroImage.

[5]  J. Wallis.  Orbitofrontal cortex and its contribution to decision-making. , 2007, Annual review of neuroscience.

[6]  Denise Brandão de Oliveira e Britto,et al.  The faculty of language , 2007 .

[7]  R. Andersen,et al.  Responses to auditory stimuli in macaque lateral intraparietal area. II. Behavioral modulation. , 1999, Journal of neurophysiology.

[8]  Brian B. Avants,et al.  Symmetric diffeomorphic image registration with cross-correlation: Evaluating automated labeling of elderly and neurodegenerative brain , 2008, Medical Image Anal..

[9]  Marzio Gerbella,et al.  Multimodal architectonic subdivision of the rostral part (area F5) of the macaque ventral premotor cortex , 2009, The Journal of comparative neurology.

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

[11]  D. Moody,et al.  Frequency selectivity of the monkey's auditory system: psychophysical tuning curves. , 1982, The Journal of the Acoustical Society of America.

[12]  A. Schleicher,et al.  Broca's region revisited: Cytoarchitecture and intersubject variability , 1999, The Journal of comparative neurology.

[13]  Doris Y. Tsao,et al.  Patches of face-selective cortex in the macaque frontal lobe , 2008, Nature Neuroscience.

[14]  P. Matthews,et al.  Defining a left-lateralized response specific to intelligible speech using fMRI. , 2003, Cerebral cortex.

[15]  G. Orban,et al.  Visual Motion Processing Investigated Using Contrast Agent-Enhanced fMRI in Awake Behaving Monkeys , 2001, Neuron.

[16]  R. Goebel,et al.  Mirror-Symmetric Tonotopic Maps in Human Primary Auditory Cortex , 2003, Neuron.

[17]  D Yves von Cramon,et al.  Distinct fMRI responses to laughter, speech, and sounds along the human peri-sylvian cortex. , 2005, Brain research. Cognitive brain research.

[18]  N. Logothetis,et al.  A voice region in the monkey brain , 2008, Nature Neuroscience.

[19]  Franck Ramus,et al.  Interhemispheric differences in auditory processing revealed by fMRI in awake rhesus monkeys. , 2012, Cerebral cortex.

[20]  Doris Y. Tsao,et al.  Comparing face patch systems in macaques and humans , 2008, Proceedings of the National Academy of Sciences.

[21]  Anders M. Dale,et al.  Repeated fMRI Using Iron Oxide Contrast Agent in Awake, Behaving Macaques at 3 Tesla , 2002, NeuroImage.

[22]  A. Syrota,et al.  The Cortical Representation of Speech , 1993, Journal of Cognitive Neuroscience.

[23]  Guy A. Orban,et al.  Integration of shape and motion cues in biological motion processing in the monkey STS , 2012, NeuroImage.

[24]  Brian H Scott,et al.  Effect of Behavioral Context on Representation of a Spatial Cue in Core Auditory Cortex of Awake Macaques , 2007, The Journal of Neuroscience.

[25]  Marco Iacoboni,et al.  The Essential Role of Premotor Cortex in Speech Perception , 2007, Current Biology.

[26]  Guy A. Orban,et al.  Visual Activation in Prefrontal Cortex is Stronger in Monkeys than in Humans , 2004, Journal of Cognitive Neuroscience.

[27]  P. Marler,et al.  Rhesus monkey (Macaca mulatta) screams: Representational signalling in the recruitment of agonistic aid , 1984, Animal Behaviour.

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

[29]  Roy D. Patterson,et al.  Vocal-Tract Resonances as Indexical Cues in Rhesus Monkeys , 2007, Current Biology.

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

[31]  Bruno B Averbeck,et al.  Integration of Auditory and Visual Communication Information in the Primate Ventrolateral Prefrontal Cortex , 2006, The Journal of Neuroscience.

[32]  Christoph Kayser,et al.  An Auditory Region in the Primate Insular Cortex Responding Preferentially to Vocal Communication Sounds , 2009, The Journal of Neuroscience.

[33]  R. Zatorre,et al.  Human temporal-lobe response to vocal sounds. , 2002, Brain research. Cognitive brain research.

[34]  J. Rauschecker,et al.  Cortical Representation of Natural Complex Sounds: Effects of Acoustic Features and Auditory Object Category , 2010, The Journal of Neuroscience.

[35]  R. Patterson,et al.  Time-domain modeling of peripheral auditory processing: a modular architecture and a software platform. , 1995, The Journal of the Acoustical Society of America.

[36]  Gonzalo H. Otazu,et al.  Engaging in an auditory task suppresses responses in auditory cortex , 2009, Nature Neuroscience.

[37]  Sterling C. Johnson,et al.  A population-average MRI-based atlas collection of the rhesus macaque , 2009, NeuroImage.

[38]  W. Penny,et al.  ANOVAs and SPM , 2003 .

[39]  Matthew H. Davis,et al.  Hierarchical Processing in Spoken Language Comprehension , 2003, The Journal of Neuroscience.

[40]  R. Zatorre,et al.  Adaptation to speaker's voice in right anterior temporal lobe , 2003, Neuroreport.

[41]  G K Martin,et al.  Effects of reaction time performance on single-unit activity in the central auditory pathway of the rhesus macaque , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  Pascal Belin,et al.  Is voice processing species-specific in human auditory cortex? An fMRI study , 2004, NeuroImage.

[43]  Mario A Ruggero,et al.  Unexceptional sharpness of frequency tuning in the human cochlea. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[44]  G. Orban,et al.  Observing Others: Multiple Action Representation in the Frontal Lobe , 2005, Science.

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

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

[47]  M. Mishkin,et al.  Functional Mapping of the Primate Auditory System , 2003, Science.

[48]  J. Fritz,et al.  Rhesus macaques spontaneously perceive formants in conspecific vocalizations. , 2006, The Journal of the Acoustical Society of America.

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

[50]  Roel M. Willems,et al.  When language meets action: the neural integration of gesture and speech. , 2007, Cerebral cortex.

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

[52]  R. Andersen,et al.  Responses to auditory stimuli in macaque lateral intraparietal area. I. Effects of training. , 1999, Journal of neurophysiology.

[53]  D. Lewis,et al.  Mapping auditory core, lateral belt, and parabelt cortices in the human superior temporal gyrus , 2005, The Journal of comparative neurology.

[54]  N. Logothetis,et al.  A combined MRI and histology atlas of the rhesus monkey brain in stereotaxic coordinates , 2007 .

[55]  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.

[56]  P. van Dijk,et al.  Mapping the Tonotopic Organization in Human Auditory Cortex with Minimally Salient Acoustic Stimulation , 2011, Cerebral cortex.

[57]  B. Averbeck,et al.  The primate cortical auditory system and neural representation of conspecific vocalizations. , 2009, Annual review of neuroscience.

[58]  Charles H. Brown,et al.  Cross-Species Comparisons of Vocal Perception , 2012 .

[59]  P. Marler,et al.  Monkey responses to three different alarm calls: evidence of predator classification and semantic communication. , 1980, Science.

[60]  A. Liberman,et al.  The motor theory of speech perception revised , 1985, Cognition.

[61]  K. Scherer,et al.  Acoustic profiles in vocal emotion expression. , 1996, Journal of personality and social psychology.

[62]  P. Marler,et al.  Food-associated calls in rhesus macaques (Macaca mulatta): I. Socioecological factors , 1993 .

[63]  Alex Martin,et al.  Species-specific calls activate homologs of Broca's and Wernicke's areas in the macaque , 2006, Nature Neuroscience.

[64]  Simon B. Eickhoff,et al.  Analysis of neural mechanisms underlying verbal fluency in cytoarchitectonically defined stereotaxic space—The roles of Brodmann areas 44 and 45 , 2004, NeuroImage.

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

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

[67]  R. Andersen,et al.  Spatially tuned auditory responses in area LIP of macaques performing delayed memory saccades to acoustic targets. , 1996, Journal of neurophysiology.

[68]  G. Orban,et al.  Coding observed motor acts: different organizational principles in the parietal and premotor cortex of humans. , 2010, Journal of neurophysiology.

[69]  J. Kaas,et al.  Subdivisions of auditory cortex and processing streams in primates. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[70]  C Tempelmann,et al.  Electrodynamic headphones and woofers for application in magnetic resonance imaging scanners. , 1998, Medical physics.

[71]  M. Mishkin,et al.  Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex , 1999, Nature Neuroscience.

[72]  P. Denes.  On the Motor Theory of Speech Perception , 1965 .

[73]  David C. Van Essen,et al.  Application of Information Technology: An Integrated Software Suite for Surface-based Analyses of Cerebral Cortex , 2001, J. Am. Medical Informatics Assoc..

[74]  Beng Hong. Goh,et al.  Effects of training. , 2001 .

[75]  Lizabeth M Romanski,et al.  Domain specificity in the primate prefrontal cortex , 2004, Cognitive, affective & behavioral neuroscience.

[76]  Asif A Ghazanfar,et al.  Interactions between the Superior Temporal Sulcus and Auditory Cortex Mediate Dynamic Face/Voice Integration in Rhesus Monkeys , 2008, The Journal of Neuroscience.

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