Interhemispheric differences in auditory processing revealed by fMRI in awake rhesus monkeys.

Lesion studies in monkeys have suggested a modest left hemisphere dominance for processing species-specific vocalizations, the neural basis of which has thus far remained unclear. We used contrast agent-enhanced functional magnetic resonance imaging to map the regions of the rhesus monkey brain involved in processing conspecific vocalizations as well as human speech and emotional sounds. Control conditions included scrambled versions of all 3 stimuli and silence. Compared with silence, all stimuli activated widespread parts of the auditory cortex and subcortical auditory structures with a right hemispheric bias at the level of the auditory core. However, comparing intact with scrambled sounds revealed a leftward bias in the auditory belt and the parabelt. The left-sided dominance was stronger and more robust for human speech than for rhesus vocalizations and hence does not reflect conspecific call selectivity but rather the processing of complex spectrotemporal patterns, such as those present in human speech and in some of the rhesus monkey vocalizations. This was confirmed by regressing brain activity with a model-derived parameter indexing the prevalence of such patterns. Our results indicate that processing of vocal sounds in the lateral belt and parabelt is asymmetric in monkeys, as predicted from lesion studies.

[1]  G. Ehret Left hemisphere advantage in the mouse brain for recognizing ultrasonic communication calls , 1987, Nature.

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

[3]  Biao Tian,et al.  Processing of frequency-modulated sounds in the lateral auditory belt cortex of the rhesus monkey. , 2004, Journal of neurophysiology.

[4]  J. Kaas,et al.  Architectonic identification of the core region in auditory cortex of macaques, chimpanzees, and humans , 2001, The Journal of comparative neurology.

[5]  H. Heffner,et al.  Hearing loss in Japanese macaques following bilateral auditory cortex lesions. , 1986, Journal of neurophysiology.

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

[7]  H. Kennedy,et al.  Anatomical Evidence of Multimodal Integration in Primate Striate Cortex , 2002, The Journal of Neuroscience.

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

[9]  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.

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

[11]  Asif A. Ghazanfar,et al.  The Role of Temporal Cues in Rhesus Monkey Vocal Recognition: Orienting Asymmetries to Reversed Calls , 2002, Brain, Behavior and Evolution.

[12]  Yale E Cohen,et al.  Coding of auditory-stimulus identity in the auditory non-spatial processing stream. , 2008, Journal of neurophysiology.

[13]  Pascal Belin,et al.  Human cerebral response to animal affective vocalizations , 2008, Proceedings of the Royal Society B: Biological Sciences.

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

[15]  Arno Klein,et al.  Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration , 2009, NeuroImage.

[16]  William C. Stebbins,et al.  The significant features of Japanese macaque coo sounds: a psychophysical study , 1988, Animal Behaviour.

[17]  S. Scott,et al.  Converging Language Streams in the Human Temporal Lobe , 2006, The Journal of Neuroscience.

[18]  Asif A Ghazanfar,et al.  Dynamic, rhythmic facial expressions and the superior temporal sulcus of macaque monkeys: implications for the evolution of audiovisual speech , 2010, The European journal of neuroscience.

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

[20]  C. Schroeder,et al.  Speech-evoked activity in primary auditory cortex: effects of voice onset time. , 1994, Electroencephalography and clinical neurophysiology.

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

[22]  L Weiskrantz,et al.  Disruptions of auditory sequence discrimination by unilateral and bilateral cortical ablations of superior temporal gyrus in the monkey. , 1970, Experimental neurology.

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

[24]  Pascal Belin,et al.  Stimulus Complexity and Categorical Effects in Human Auditory Cortex: An Activation Likelihood Estimation Meta-Analysis , 2011, Front. Psychology.

[25]  Guy A. Orban,et al.  The monkey ventral premotor cortex processes 3D shape from disparity , 2009, NeuroImage.

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

[27]  D B Moody,et al.  Categorical perception of conspecific communication sounds by Japanese macaques, Macaca fuscata. , 1989, The Journal of the Acoustical Society of America.

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

[29]  Bruno B Averbeck,et al.  Probabilistic Encoding of Vocalizations in Macaque Ventral Lateral Prefrontal Cortex , 2006, The Journal of Neuroscience.

[30]  J. Rauschecker,et al.  Functional Specialization in Rhesus Monkey Auditory Cortex , 2001, Science.

[31]  Marko Wilke,et al.  LI-tool: A new toolbox to assess lateralization in functional MR-data , 2007, Journal of Neuroscience Methods.

[32]  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.

[33]  D. Bendor,et al.  The neuronal representation of pitch in primate auditory cortex , 2005, Nature.

[34]  Svetlana S. Georgieva,et al.  The Processing of Three-Dimensional Shape from Disparity in the Human Brain , 2009, The Journal of Neuroscience.

[35]  G. Orban,et al.  Charting the Lower Superior Temporal Region, a New Motion-Sensitive Region in Monkey Superior Temporal Sulcus , 2006, The Journal of Neuroscience.

[36]  Jack W. Bradbury,et al.  Principles of Animal Communication , 1998 .

[37]  Marc D Hauser,et al.  Vervet monkeys and humans show brain asymmetries for processing conspecific vocalizations, but with opposite patterns of laterality , 2006, Proceedings of the Royal Society B: Biological Sciences.

[38]  Asif A. Ghazanfar,et al.  Language Evolution: Loquacious Monkey Brains? , 2006, Current Biology.

[39]  S A Shamma,et al.  Spectro-temporal response field characterization with dynamic ripples in ferret primary auditory cortex. , 2001, Journal of neurophysiology.

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

[41]  K H Pribram,et al.  Effects of ablations of temporal cortex upon speech sound discrimination in the monkey. , 1969, Experimental neurology.

[42]  Marion Smits,et al.  Activation of Cortical and Subcortical Auditory Structures at 3 T by Means of a Functional Magnetic Resonance Imaging Paradigm Suitable for Clinical Use , 2006, Investigative radiology.

[43]  A. Puce,et al.  Neuronal oscillations and visual amplification of speech , 2008, Trends in Cognitive Sciences.

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

[45]  N. Logothetis,et al.  Frontiers in Integrative Neuroscience Integrative Neuroscience Directed Interactions between Auditory and Superior Temporal Cortices and Their Role in Sensory Integration , 2022 .

[46]  Ventrolateral Prefrontal Cortex and Controlling Memory to Inform Action , 2007 .

[47]  D. M. Green,et al.  Intensity discrimination as a function of frequency and sensation level. , 1977, The Journal of the Acoustical Society of America.

[48]  Y. Cohen,et al.  Discrimination of Functionally Referential Calls by Laboratory-Housed Rhesus Macaques: Implications for Neuroethological Studies , 2003, Brain, Behavior and Evolution.

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

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

[51]  Kenneth Webb,et al.  Evolution of Communication Simulation of Adaptive Behavior – Project Report , 2004 .

[52]  H. Heffner,et al.  Temporal lobe lesions and perception of species-specific vocalizations by macaques. , 1984, Science.

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

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

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

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

[57]  J. Rauschecker Parallel Processing in the Auditory Cortex of Primates , 1998, Audiology and Neurotology.

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

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

[60]  G. Rizzolatti,et al.  ß Federation of European Neuroscience Societies Mirror , 2003 .

[61]  D. Moody,et al.  Neural lateralization of species-specific vocalizations by Japanese macaques (Macaca fuscata). , 1978, Science.

[62]  Patrick R. Hof,et al.  Leftward interhemispheric asymmetry of macaque monkey temporal lobe language area homolog is evident at the cytoarchitectural, but not gross anatomic level , 2008, Brain Research.

[63]  J. Rauschecker,et al.  Mechanisms and streams for processing of "what" and "where" in auditory cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[66]  Willy Serniclaes,et al.  Neural correlates of switching from auditory to speech perception , 2005, NeuroImage.

[67]  Maneesh C. Patel,et al.  Perceptual Systems Controlling Speech Production , 2008, The Journal of Neuroscience.

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

[69]  D. V. von Cramon,et al.  Orienting asymmetries and lateralized processing of sounds in humans , 2009, BMC Neuroscience.

[70]  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.

[71]  J. Kaas,et al.  Subdivisions of auditory cortex and ipsilateral cortical connections of the parabelt auditory cortex in macaque monkeys , 1998, The Journal of comparative neurology.

[72]  J. H. Dewson,et al.  Effects of unilateral ablation of superior temporal cortex on auditory sequence discrimination in Macaca mulatta. , 1972, Neuropsychologia.

[73]  J. Kaas,et al.  Prefrontal connections of the parabelt auditory cortex in macaque monkeys , 1999, Brain Research.

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

[75]  M. Hauser,et al.  Left hemisphere dominance for processing vocalizations in adult, but not infant, rhesus monkeys: field experiments. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[78]  T. Wagner,et al.  Categorical discrimination of direction in frequency-modulated tones by Mongolian gerbils , 1998, Behavioural Brain Research.

[79]  N. Logothetis,et al.  Functional Imaging Reveals Numerous Fields in the Monkey Auditory Cortex , 2006, PLoS biology.

[80]  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.

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

[82]  P. Roelfsema,et al.  Bottom-Up Dependent Gating of Frontal Signals in Early Visual Cortex , 2008, Science.

[83]  A. Ghazanfar,et al.  On the relationship between lateralized brain function and orienting asymmetries. , 2010, Behavioral neuroscience.

[84]  H. Heffner,et al.  An investigation of sensory deficits underlying the aphasia-like behavior of macaques with auditory cortex lesions , 2001, Neuroreport.

[85]  S. Scott,et al.  Identification of a pathway for intelligible speech in the left temporal lobe. , 2000, Brain : a journal of neurology.

[86]  H. Heffner,et al.  Effect of restricted cortical lesions on absolute thresholds and aphasia-like deficits in Japanese macaques. , 1989, Behavioral neuroscience.

[87]  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.