Cerebral Processing of Voice Gender Studied Using a Continuous Carryover fMRI Design

Normal listeners effortlessly determine a person's gender by voice, but the cerebral mechanisms underlying this ability remain unclear. Here, we demonstrate 2 stages of cerebral processing during voice gender categorization. Using voice morphing along with an adaptation-optimized functional magnetic resonance imaging design, we found that secondary auditory cortex including the anterior part of the temporal voice areas in the right hemisphere responded primarily to acoustical distance with the previously heard stimulus. In contrast, a network of bilateral regions involving inferior prefrontal and anterior and posterior cingulate cortex reflected perceived stimulus ambiguity. These findings suggest that voice gender recognition involves neuronal populations along the auditory ventral stream responsible for auditory feature extraction, functioning in pair with the prefrontal cortex in voice gender perception.

[1]  Jonathan D. Cohen,et al.  Anterior Cingulate Conflict Monitoring and Adjustments in Control , 2004, Science.

[2]  Lynn M. Farnsworth,et al.  The perceptual representation of voice gender. , 1995, The Journal of the Acoustical Society of America.

[3]  D G Childers,et al.  Gender recognition from speech. Part II: Fine analysis. , 1991, The Journal of the Acoustical Society of America.

[4]  A. Nakamura,et al.  Neural substrates for recognition of familiar voices: a PET study , 2001, Neuropsychologia.

[5]  Leslie G. Ungerleider,et al.  A general mechanism for perceptual decision-making in the human brain , 2004, Nature.

[6]  M. Gazzaniga.  Interview with Michael Gazzaniga , 2011, Annals of the New York Academy of Sciences.

[7]  Muge M. Bakircioglu,et al.  Mapping visual cortex in monkeys and humans using surface-based atlases , 2001, Vision Research.

[8]  D. Childers,et al.  Gender recognition from speech. Part I: Coarse analysis. , 1991, The Journal of the Acoustical Society of America.

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

[10]  M. Botvinick,et al.  Anterior cingulate cortex, error detection, and the online monitoring of performance. , 1998, Science.

[11]  J. Armony,et al.  Sensitivity to voice in human prefrontal cortex. , 2005, Journal of neurophysiology.

[12]  Yale E Cohen,et al.  Spontaneous processing of abstract categorical information in the ventrolateral prefrontal cortex , 2006, Biology Letters.

[13]  M. Corbetta,et al.  Common Blood Flow Changes across Visual Tasks: II. Decreases in Cerebral Cortex , 1997, Journal of Cognitive Neuroscience.

[14]  Hideki Kawahara,et al.  STRAIGHT, exploitation of the other aspect of VOCODER: Perceptually isomorphic decomposition of speech sounds , 2006 .

[15]  C. Theobald,et al.  Design sequences for sensory studies: achieving balance for carry-over and position effects. , 2007, The British journal of mathematical and statistical psychology.

[16]  K. Grill-Spector,et al.  fMR-adaptation: a tool for studying the functional properties of human cortical neurons. , 2001, Acta psychologica.

[17]  A. Nakamura,et al.  Vocal identification of speaker and emotion activates differerent brain regions , 1997, Neuroreport.

[18]  J. Hillenbrand,et al.  Acoustic characteristics of American English vowels. , 1994, The Journal of the Acoustical Society of America.

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

[20]  M. Corbetta,et al.  Common Blood Flow Changes across Visual Tasks: I. Increases in Subcortical Structures and Cerebellum but Not in Nonvisual Cortex , 1997, Journal of Cognitive Neuroscience.

[21]  James M. McQueen,et al.  Neural mechanisms for voice recognition , 2010, NeuroImage.

[22]  Hideki Kawahara.  Exemplar-based Voice Quality Analysis and Control using a High Quality Auditory Morphing Procedure based on STRAIGHT Hideki Kawahara , 2003 .

[23]  G. Boynton,et al.  Adaptation: from single cells to BOLD signals , 2006, Trends in Neurosciences.

[24]  Cameron S Carter,et al.  Stimulus and response conflict processing during perceptual decision making , 2009, Cognitive, affective & behavioral neuroscience.

[25]  J. Mullennix,et al.  Talker Variability in Speech Processing , 1997 .

[26]  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..

[27]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[28]  R. Zatorre,et al.  Sensitivity to Auditory Object Features in Human Temporal Neocortex , 2004, The Journal of Neuroscience.

[29]  A. Ghazanfar,et al.  Evolution of human vocal production , 2008, Current Biology.

[30]  Hideki Kawahara,et al.  Auditory Adaptation in Voice Perception , 2008, Current Biology.

[31]  T. Johnstone,et al.  The voice of emotion: an FMRI study of neural responses to angry and happy vocal expressions. , 2006, Social cognitive and affective neuroscience.

[32]  Geoffrey Karl Aguirre,et al.  Continuous carry-over designs for fMRI , 2007, NeuroImage.

[33]  Dave R. M. Langers,et al.  fMRI activation in relation to sound intensity and loudness , 2007, NeuroImage.

[34]  Marco Iacoboni,et al.  The self across the senses: an fMRI study of self-face and self-voice recognition. , 2008, Social cognitive and affective neuroscience.

[35]  Thomas A. Zeffiro,et al.  The influences of task difficulty and response correctness on neural systems supporting fluid reasoning , 2007, Cognitive Neurodynamics.

[36]  Leslie G. Ungerleider,et al.  The neural systems that mediate human perceptual decision making , 2008, Nature Reviews Neuroscience.

[37]  Rainer Goebel,et al.  "Who" Is Saying "What"? Brain-Based Decoding of Human Voice and Speech , 2008, Science.

[38]  Nikolaus Kriegeskorte,et al.  Face-identity change activation outside the face system: "release from adaptation" may not always indicate neuronal selectivity. , 2010, Cerebral cortex.

[39]  M. Andrews,et al.  Gender presentation: perceptual and acoustical analyses of voice. , 1997, Journal of voice : official journal of the Voice Foundation.

[40]  Wolfgang Grodd,et al.  Identification of emotional intonation evaluated by fMRI , 2005, NeuroImage.

[41]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[42]  Michael D. Hunter,et al.  Male and female voices activate distinct regions in the male brain , 2005, NeuroImage.

[43]  Michael Erb,et al.  Impact of voice on emotional judgment of faces: An event‐related fMRI study , 2006, Human brain mapping.

[44]  David A. Medler,et al.  Neural correlates of sensory and decision processes in auditory object identification , 2004, Nature Neuroscience.

[45]  Jonathan D. Cohen,et al.  Conflict monitoring versus selection-for-action in anterior cingulate cortex , 1999, Nature.

[46]  N. Logothetis.  What we can do and what we cannot do with fMRI , 2008, Nature.

[47]  Angela D Friederici,et al.  � Human Brain Mapping 24:11–20(2005) � Voice Perception: Sex, Pitch, and the Right Hemisphere , 2022 .

[48]  K. Grill-Spector,et al.  Repetition and the brain: neural models of stimulus-specific effects , 2006, Trends in Cognitive Sciences.

[49]  Pascal Belin,et al.  Learning-induced changes in the cerebral processing of voice identity. , 2011, Cerebral cortex.

[50]  T Murry,et al.  Multidimensional analysis of male and female voices. , 1980, The Journal of the Acoustical Society of America.

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

[52]  P. C. Murphy,et al.  Cerebral Cortex , 2017, Cerebral Cortex.

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

[54]  J. Binder,et al.  A Parametric Manipulation of Factors Affecting Task-induced Deactivation in Functional Neuroimaging , 2003, Journal of Cognitive Neuroscience.

[55]  Michael Erb,et al.  Cerebral pathways in processing of affective prosody: A dynamic causal modeling study , 2006, NeuroImage.