The Superior Temporal Sulcus Differentiates Communicative and Noncommunicative Auditory Signals

Processing the vocalizations of conspecifics is critical for adaptive social interaction. A species-specific voice-selective region has been identified in the right STS that responds more strongly to human vocal sounds compared with a variety of nonvocal sounds. However, the STS also activates in response to a wide range of signals used in communication, such as eye gaze, biological motion, and speech. These findings raise the possibility that the voice-selective region of the STS may be especially sensitive to vocal sounds that are communicative, rather than to all human vocal sounds. Using fMRI, we demonstrate that the voice-selective region of the STS responds more strongly to communicative vocal sounds (such as speech and laughter) compared with noncommunicative vocal sounds (such as coughing and sneezing). The implications of these results for understanding the role of the STS in voice processing and in disorders of social communication, such as autism spectrum disorder, are discussed.

[1]  D. Perrett,et al.  A region of right posterior superior temporal sulcus responds to observed intentional actions , 2004, Neuropsychologia.

[2]  Pascal Belin,et al.  Abnormal cortical voice processing in autism , 2004, Nature Neuroscience.

[3]  T. Allison,et al.  Social perception from visual cues: role of the STS region , 2000, Trends in Cognitive Sciences.

[4]  Anne-Lise Giraud,et al.  Distinct functional substrates along the right superior temporal sulcus for the processing of voices , 2004, NeuroImage.

[5]  G. McCarthy,et al.  Dynamic perception of facial affect and identity in the human brain. , 2003, Cerebral Cortex.

[6]  H. Grice.  Utterer’s Meaning, Sentence-Meaning, and Word-Meaning , 1968 .

[7]  Uta Frith,et al.  Theory of mind , 2001, Current Biology.

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

[9]  Geraldine Dawson,et al.  Links between social and linguistic processing of speech in preschool children with autism: behavioral and electrophysiological measures. , 2005, Developmental science.

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

[11]  Gregory McCarthy,et al.  Perceived causality influences brain activity evoked by biological motion , 2008, Social neuroscience.

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

[13]  Ivan Toni,et al.  A Dissociation Between Linguistic and Communicative Abilities in the Human Brain , 2010, Psychological science.

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

[15]  M. Hauser.  A primate dictionary? decoding the function and meaning of another species’ vocalizations , 2000 .

[16]  Jiang Xu,et al.  Language in context: emergent features of word, sentence, and narrative comprehension , 2005, NeuroImage.

[17]  Aina Puce,et al.  Electrophysiology and brain imaging of biological motion. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[18]  Robert T. Knight,et al.  Superior Temporal SulcusIt's My Area: Or Is It? , 2008, Journal of Cognitive Neuroscience.

[19]  Donald J. Cohen,et al.  Comprehension of indirect requests in adults with autistic disorders and mental retardation. , 1985, Journal of speech and hearing research.

[20]  Teemu Rinne,et al.  Stimulus-dependent activations and attention-related modulations in the auditory cortex: A meta-analysis of fMRI studies , 2014, Hearing Research.

[21]  S. Baron-Cohen,et al.  Reading the Mind in the Voice: A Study with Normal Adults and Adults with Asperger Syndrome and High Functioning Autism , 2002, Journal of autism and developmental disorders.

[22]  C. Frith,et al.  Functional imaging of ‘theory of mind’ , 2003, Trends in Cognitive Sciences.

[23]  C. Price.  The anatomy of language: contributions from functional neuroimaging , 2000, Journal of anatomy.

[24]  M. Tomasello.  Origins of human communication , 2008 .

[25]  Karsten Specht,et al.  Functional segregation of the temporal lobes into highly differentiated subsystems for auditory perception: an auditory rapid event-related fMRI-task , 2003, NeuroImage.

[26]  F. Rösler,et al.  Brain Activation Modulated by the Comprehension of Normal and Pseudo-word Sentences of Different Processing Demands: A Functional Magnetic Resonance Imaging Study , 2002, NeuroImage.

[27]  R. Saxe.  Uniquely human social cognition , 2006, Current Opinion in Neurobiology.

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

[29]  J. Haxby,et al.  The distributed human neural system for face perception , 2000, Trends in Cognitive Sciences.

[30]  Arcangelo Merla,et al.  Infant cortex responds to other humans from shortly after birth , 2013, Scientific Reports.

[31]  Charles J. Lynch,et al.  Underconnectivity between voice-selective cortex and reward circuitry in children with autism , 2013, Proceedings of the National Academy of Sciences.

[32]  R. Johnstone,et al.  Animal signals , 2013, Current Biology.

[33]  Mikko Sams,et al.  Perceiving identical sounds as speech or non-speech modulates activity in the left posterior superior temporal sulcus , 2006, NeuroImage.

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

[35]  F. Manes,et al.  Action-verb processing in Parkinson’s disease: new pathways for motor–language coupling , 2013, Brain Structure and Function.

[36]  S. Campanella,et al.  Integrating face and voice in person perception , 2007, Trends in Cognitive Sciences.

[37]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[38]  M. Sabbagh.  Communicative Intentions and Language: Evidence from Right-Hemisphere Damage and Autism , 1999, Brain and Language.

[39]  Ami Klin,et al.  Young autistic children's listening preferences in regard to speech: A possible characterization of the symptom of social withdrawal , 1991, Journal of autism and developmental disorders.

[40]  J. Haxby,et al.  Distinct representations of eye gaze and identity in the distributed human neural system for face perception , 2000, Nature Neuroscience.

[41]  T. Allison,et al.  Brain Activity Evoked by the Perception of Human Walking: Controlling for Meaningful Coherent Motion , 2003, The Journal of Neuroscience.

[42]  E. Redcay.  The superior temporal sulcus performs a common function for social and speech perception: Implications for the emergence of autism , 2008, Neuroscience & Biobehavioral Reviews.

[43]  Nathalie Boddaert,et al.  Autism, the superior temporal sulcus and social perception , 2006, Trends in Neurosciences.

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

[45]  K. Kiehl,et al.  Detection of Sounds in the Auditory Stream: Event-Related fMRI Evidence for Differential Activation to Speech and Nonspeech , 2001, Journal of Cognitive Neuroscience.

[46]  Danielle Z. Bolling,et al.  fNIRS detects temporal lobe response to affective touch. , 2014, Social cognitive and affective neuroscience.