Is voice processing species-specific in human auditory cortex? An fMRI study

Recent studies suggested a sensitivity of regions of the human superior temporal sulcus (STS) to the sound of the human voice. However, the question of the species specificity of this response is still open. Healthy adult volunteers were scanned in an event-related fMRI design to compare responses in the STS to human and animal vocalizations, as well as to control nonvocal sounds (e.g., musical instruments). Bilateral activation of anterior STS was observed for human vocalizations, when contrasted with both nonvocal sounds and animal vocalizations. Animal vocalizations, compared to nonvocal sounds, elicited a more restricted left STS activation, although this region responded even more strongly to human vocalizations. This study provides the first evidence suggesting a species specificity in STS responses to vocalizations in humans.

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

[2]  J. Newman,et al.  Auditory Cortex of Squirrel Monkey: Response Patterns of Single Cells to Species-Specific Vocalizations , 1972, Science.

[3]  S. Green,et al.  Variation of Vocal Pattern with Social Situation in the Japanese Monkey (Macaca fuscata): A Field Study * , 1975 .

[4]  R. Andrew,et al.  The origin and evolution of the calls and facial expressions of the primates. , 1963 .

[5]  D. Rendall.  Acoustic correlates of caller identity and affect intensity in the vowel-like grunt vocalizations of baboons. , 2003, The Journal of the Acoustical Society of America.

[6]  Phyllis C. Jay,et al.  Primates: Studies in Adaptation and Variability , 1968 .

[7]  I. Gauthier,et al.  Expertise for cars and birds recruits brain areas involved in face recognition , 2000, Nature Neuroscience.

[8]  N. Kanwisher,et al.  How Distributed Is Visual Category Information in Human Occipito-Temporal Cortex? An fMRI Study , 2002, Neuron.

[9]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

[10]  R. Dolan,et al.  Modulation of spatial attention by fear-conditioned stimuli: an event-related fMRI study , 2002, Neuropsychologia.

[11]  S. Altmann,et al.  Social communication among primates , 1967 .

[12]  D. Ploog,et al.  Vocal repertoire of the squirrel monkey (Saimiri sciureus), its analysis and significance , 2004, Experimental Brain Research.

[13]  G. Bydder,et al.  Magnetic Resonance Scanning and Epilepsy , 1994, NATO ASI Series.

[14]  D. Fossey,et al.  Vocalizations of the mountain Gorilla (Gorilla gorilla beringei) , 1972 .

[15]  T. Allison,et al.  Face-Specific Processing in the Human Fusiform Gyrus , 1997, Journal of Cognitive Neuroscience.

[16]  Jorge L. Armony,et al.  Modulation of auditory neural responses by a visual context in human fear conditioning , 2001, Neuroreport.

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

[18]  Xiaoqin Wang,et al.  Differential representation of species-specific primate vocalizations in the auditory cortices of marmoset and cat. , 2001, Journal of neurophysiology.

[19]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[20]  M M Merzenich,et al.  Representation of a species-specific vocalization in the primary auditory cortex of the common marmoset: temporal and spectral characteristics. , 1995, Journal of neurophysiology.

[21]  J. Thiran,et al.  Distinct Pathways Involved in Sound Recognition and Localization: A Human fMRI Study , 2000, NeuroImage.

[22]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited—Again , 1995, NeuroImage.

[23]  N. Kanwisher,et al.  The fusiform face area is selective for faces not animals. , 1999, Neuroreport.

[24]  Arvid Kappas,et al.  Primate Vocal Expression of Affective State , 1988 .

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

[26]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[27]  Philipp Goedeking,et al.  Primate Vocal Communication , 1988, Springer Berlin Heidelberg.

[28]  Alan C. Evans,et al.  An MRI-Based Probabilistic Atlas of Neuroanatomy , 1994 .

[29]  Thomas A. Sebeok,et al.  How Animals Communicate , 1979 .

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

[31]  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.

[32]  S. Carey,et al.  Why faces are and are not special: an effect of expertise. , 1986, Journal of experimental psychology. General.

[33]  J P Rauschecker,et al.  Processing of frequency-modulated sounds in the cat's posterior auditory field. , 1994, Journal of neurophysiology.

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

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

[36]  E. Halgren,et al.  Cognitive response profile of the human fusiform face area as determined by MEG. , 2000, Cerebral cortex.

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

[38]  P. Belin,et al.  Thinking the voice: neural correlates of voice perception , 2004, Trends in Cognitive Sciences.

[39]  N. Kanwisher.  Domain specificity in face perception , 2000, Nature Neuroscience.

[40]  J. Newman,et al.  Multiple coding of species-specific vocalizations in the auditory cortex of squirrel monkeys. , 1973, Brain research.

[41]  C. Grady,et al.  “What” and “where” in the human auditory system , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[42]  M. Tarr,et al.  FFA: a flexible fusiform area for subordinate-level visual processing automatized by expertise , 2000, Nature Neuroscience.