Superior Temporal SulcusIt's My Area: Or Is It?

The superior temporal sulcus (STS) is the chameleon of the human brain. Several research areas claim the STS as the host brain region for their particular behavior of interest. Some see it as one of the core structures for theory of mind. For others, it is the main region for audiovisual integration. It plays an important role in biological motion perception, but is also claimed to be essential for speech processing and processing of faces. We review the foci of activations in the STS from multiple functional magnetic resonance imaging studies, focusing on theory of mind, audiovisual integration, motion processing, speech processing, and face processing. The results indicate a differentiation of the STS region in an anterior portion, mainly involved in speech processing, and a posterior portion recruited by cognitive demands of all these different research areas. The latter finding argues against a strict functional subdivision of the STS. In line with anatomical evidence from tracer studies, we propose that the function of the STS varies depending on the nature of network coactivations with different regions in the frontal cortex and medial-temporal lobe. This view is more in keeping with the notion that the same brain region can support different cognitive operations depending on task-dependent network connections, emphasizing the role of network connectivity analysis in neuroimaging.

[1]  Robert T. Knight,et al.  Temporal Characteristics of Audiovisual Information Processing , 2008, The Journal of Neuroscience.

[2]  Kenneth Hugdahl,et al.  Processing of sub-syllabic speech units in the posterior temporal lobe: An fMRI study , 2005, NeuroImage.

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

[4]  R. Blake,et al.  Brain Areas Active during Visual Perception of Biological Motion , 2002, Neuron.

[5]  Norihiro Sadato,et al.  Role of the superior temporal region in human visual motion perception. , 2005, Cerebral cortex.

[6]  L. Tyler,et al.  Binding crossmodal object features in perirhinal cortex. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[7]  H. Barbas.  Connections underlying the synthesis of cognition, memory, and emotion in primate prefrontal cortices , 2000, Brain Research Bulletin.

[8]  Rebecca Elliott,et al.  Neuronal correlates of theory of mind and empathy: A functional magnetic resonance imaging study in a nonverbal task , 2006, NeuroImage.

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

[10]  James H. Dulebohn,et al.  The biological bases of unfairness: Neuroimaging evidence for the distinctiveness of procedural and distributive justice , 2009 .

[11]  Alan C. Evans,et al.  Lateralization of phonetic and pitch discrimination in speech processing. , 1992, Science.

[12]  Jason P. Mitchell.  Activity in right temporo-parietal junction is not selective for theory-of-mind. , 2008, Cerebral cortex.

[13]  Lee M. Miller,et al.  Measuring temporal dynamics of functional networks using phase spectrum of fMRI data , 2005, NeuroImage.

[14]  Richard S. J. Frackowiak,et al.  The anatomy of phonological and semantic processing in normal subjects. , 1992, Brain : a journal of neurology.

[15]  P. Sinha,et al.  Functional neuroanatomy of biological motion perception in humans , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[16]  B. Seltzer,et al.  Architectonics and cortical connections of the upper bank of the superior temporal sulcus in the rhesus monkey: An analysis in the tangential plane , 2003, The Journal of comparative neurology.

[17]  H. Kashima,et al.  A deficit in discriminating gaze direction in a case with right superior temporal gyrus lesion , 2006, Neuropsychologia.

[18]  Ingrid R. Olson,et al.  Social cognition and the anterior temporal lobes , 2010, NeuroImage.

[19]  M. Berger,et al.  High Gamma Power Is Phase-Locked to Theta Oscillations in Human Neocortex , 2006, Science.

[20]  J C Mazziotta,et al.  Reafferent copies of imitated actions in the right superior temporal cortex , 2001, Proceedings of the National Academy of Sciences of the United States of America.

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

[22]  Roel M. Willems,et al.  Differential roles for left inferior frontal and superior temporal cortex in multimodal integration of action and language , 2009, NeuroImage.

[23]  C. Wernicke.  Der aphasische Symptomenkomplex , 1974 .

[24]  C. Nelson,et al.  Tuning the developing brain to social signals of emotions , 2009, Nature Reviews Neuroscience.

[25]  Vincent Walsh,et al.  Distinct neural substrates for visual search amongst spatial versus temporal distractors. , 2003, Brain research. Cognitive brain research.

[26]  D. Perrett,et al.  Responses of Anterior Superior Temporal Polysensory (STPa) Neurons to Biological Motion Stimuli , 1994, Journal of Cognitive Neuroscience.

[27]  Emiliano Macaluso,et al.  Spatial attention can modulate audiovisual integration at multiple cortical and subcortical sites , 2009, The European journal of neuroscience.

[28]  D. Pandya,et al.  Parietal, temporal, and occipita projections to cortex of the superior temporal sulcus in the rhesus monkey: A retrograde tracer study , 1994, The Journal of comparative neurology.

[29]  C. Büchel,et al.  Modulation of connectivity in visual pathways by attention: cortical interactions evaluated with structural equation modelling and fMRI. , 1997, Cerebral cortex.

[30]  Aina Puce,et al.  Configural Processing of Biological Motion in Human Superior Temporal Sulcus , 2005, The Journal of Neuroscience.

[31]  R. Goebel,et al.  Integration of Letters and Speech Sounds in the Human Brain , 2004, Neuron.

[32]  Swann Pichon,et al.  Two different faces of threat. Comparing the neural systems for recognizing fear and anger in dynamic body expressions , 2009, NeuroImage.

[33]  Leslie G. Ungerleider,et al.  Multiple visual areas in the caudal superior temporal sulcus of the macaque , 1986, The Journal of comparative neurology.

[34]  Conny F. Schmidt,et al.  Face perception is mediated by a distributed cortical network , 2005, Brain Research Bulletin.

[35]  Tetsuya Matsuda,et al.  Brain activation associated with evaluative processes of guilt and embarrassment: an fMRI study , 2004, NeuroImage.

[36]  J. Price,et al.  Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys , 1995, The Journal of comparative neurology.

[37]  N. Dronkers,et al.  Lesion analysis of the brain areas involved in language comprehension , 2004, Cognition.

[38]  S. Iversen,et al.  Detection of Audio-Visual Integration Sites in Humans by Application of Electrophysiological Criteria to the BOLD Effect , 2001, NeuroImage.

[39]  J. Peacock.  Two-dimensional goodness-of-fit testing in astronomy , 1983 .

[40]  D. Pandya,et al.  Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey , 2002, The European journal of neuroscience.

[41]  R. Campbell,et al.  Evidence from functional magnetic resonance imaging of crossmodal binding in the human heteromodal cortex , 2000, Current Biology.

[42]  M. Torrens.  Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[43]  J. Kaiser,et al.  Object Familiarity and Semantic Congruency Modulate Responses in Cortical Audiovisual Integration Areas , 2007, The Journal of Neuroscience.

[44]  W. Singer,et al.  Modulation of Neuronal Interactions Through Neuronal Synchronization , 2007, Science.

[45]  Karl J. Friston,et al.  The effect of prior visual information on recognition of speech and sounds. , 2008, Cerebral cortex.

[46]  D. Pandya,et al.  Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey , 1978, Brain Research.

[47]  M G Woldorff,et al.  Hemispheric asymmetries for different components of global/local attention occur in distinct temporo-parietal loci. , 2005, Cerebral cortex.

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

[49]  K. Richard,et al.  Adsorption of Palm Oil Carotene and Free Fatty Acids onto Acid Activated Cameroonian Clays , 2007 .

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

[51]  P. Fries.  A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

[52]  J. Price,et al.  Sensory and premotor connections of the orbital and medial prefrontal cortex of macaque monkeys , 1995, The Journal of comparative neurology.

[53]  Ulrike M. Krämer,et al.  Emotional and cognitive aspects of empathy and their relation to social cognition—an fMRI-study , 2010, Brain Research.

[54]  John H. R. Maunsell,et al.  The middle temporal visual area in the macaque: Myeloarchitecture, connections, functional properties and topographic organization , 1981, The Journal of comparative neurology.

[55]  D. Pandya,et al.  Frontal lobe connections of the superior temporal sulcus in the rhesus monkey , 1989, The Journal of comparative neurology.

[56]  Michael D. Rugg,et al.  Dissociation of the neural correlates of visual and auditory contextual encoding , 2010, Neuropsychologia.

[57]  Ryu-ichiro Hashimoto,et al.  An fMRI study of functional abnormalities in the verbal working memory system and the relationship to clinical symptoms in chronic schizophrenia. , 2010, Cerebral cortex.

[58]  A. Kingstone,et al.  Human Social Attention , 2009, Annals of the New York Academy of Sciences.

[59]  G. Orban,et al.  Specificity of regions processing biological motion , 2005, The European journal of neuroscience.

[60]  T. Allison,et al.  Functional anatomy of biological motion perception in posterior temporal cortex: an FMRI study of eye, mouth and hand movements. , 2005, Cerebral cortex.

[61]  Karl J. Friston,et al.  Activation in Posterior Superior Temporal Sulcus Parallels Parameter Inducing the Percept of Animacy , 2005, Neuron.

[62]  Marija J. Norusis,et al.  SPSS 16.0 Statistical Procedures Companion , 2003 .

[63]  Kosha Ruparel,et al.  Frontolimbic responses to emotional face memory: The neural correlates of first impressions , 2009, Human brain mapping.

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

[65]  Karl J. Friston,et al.  Hierarchical Processing of Auditory Objects in Humans , 2007, PLoS Comput. Biol..

[66]  G. Johansson.  Visual perception of biological motion and a model for its analysis , 1973 .

[67]  P. Fonlupt,et al.  Functional and effective connectivity in an fMRI study of an auditory‐related task , 2006, The European journal of neuroscience.

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

[69]  Clayton E. Curtis,et al.  Coherence between fMRI time-series distinguishes two spatial working memory networks , 2005, NeuroImage.

[70]  Michael S Beauchamp,et al.  See me, hear me, touch me: multisensory integration in lateral occipital-temporal cortex , 2005, Current Opinion in Neurobiology.

[71]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

[72]  D. Perrett,et al.  Opinion TRENDS in Cognitive Sciences Vol.8 No.11 November 2004 Demystifying social cognition: a Hebbian perspective , 2022 .

[73]  Sarah-Jayne Blakemore,et al.  Functional connectivity during a social emotion task in adolescents and in adults , 2009, The European journal of neuroscience.

[74]  G. Calvert.  Crossmodal processing in the human brain: insights from functional neuroimaging studies. , 2001, Cerebral cortex.

[75]  R. Knight.  Neural Networks Debunk Phrenology , 2007, Science.

[76]  Mariko Osaka,et al.  Individual differences in the theory of mind and superior temporal sulcus , 2009, Neuroscience Letters.

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

[78]  Robert Oostenveld,et al.  Neural Mechanisms of Visual Attention : How Top-Down Feedback Highlights Relevant Locations , 2007 .

[79]  E. Miller,et al.  Response to Comment on "Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices" , 2007, Science.

[80]  John A. Hartigan,et al.  Clustering Algorithms , 1975 .

[82]  Dana Samson,et al.  Left temporoparietal junction is necessary for representing someone else's belief , 2004, Nature Neuroscience.

[83]  Emily S. Cross,et al.  Dissociable substrates for body motion and physical experience in the human action observation network , 2009, The European journal of neuroscience.

[84]  Szabolcs Kéri,et al.  Oxytocin enhances the perception of biological motion in humans , 2009, Cognitive, affective & behavioral neuroscience.

[85]  Jan Derrfuss,et al.  Lost in localization: The need for a universal coordinate database , 2009, NeuroImage.

[86]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[87]  Steven L. Small,et al.  Listening to talking faces: motor cortical activation during speech perception , 2005, NeuroImage.

[88]  D. Pandya,et al.  Intrinsic connections and architectonics of the superior temporal sulcus in the rhesus monkey , 1989, The Journal of comparative neurology.

[89]  E. Charles Leek,et al.  Functional specialization in the supplementary motor complex , 2009, Nature Reviews Neuroscience.

[90]  Karl J. Friston,et al.  Modelling functional integration: a comparison of structural equation and dynamic causal models , 2004, NeuroImage.

[91]  Roy D. Patterson,et al.  Locating the initial stages of speech–sound processing in human temporal cortex , 2006, NeuroImage.

[92]  A. Amedi,et al.  Functional imaging of human crossmodal identification and object recognition , 2005, Experimental Brain Research.

[93]  R Saxe,et al.  People thinking about thinking people The role of the temporo-parietal junction in “theory of mind” , 2003, NeuroImage.

[94]  Stephen M. Rao,et al.  Human Brain Language Areas Identified by Functional Magnetic Resonance Imaging , 1997, The Journal of Neuroscience.

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

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

[97]  A. McIntosh,et al.  Structural modeling of functional neural pathways mapped with 2-deoxyglucose: effects of acoustic startle habituation on the auditory system , 1991, Brain Research.

[98]  Allen R. Braun,et al.  Distinguishing the processing of gestures from signs in deaf individuals: An fMRI study , 2009, Brain Research.

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

[100]  K. Zilles,et al.  Mind Reading: Neural Mechanisms of Theory of Mind and Self-Perspective , 2001, NeuroImage.

[101]  H. Karnath.  New insights into the functions of the superior temporal cortex , 2001, Nature Reviews Neuroscience.

[102]  Litvak,et al.  164 Dynamic Causal Modeling 6 . 1 , 2010 .

[103]  Robert T. Knight,et al.  Spatio-temporal information analysis of event-related BOLD responses , 2007, NeuroImage.

[104]  C. Frith,et al.  Reading the mind in cartoons and stories: an fMRI study of ‘theory of mind’ in verbal and nonverbal tasks , 2000, Neuropsychologia.

[105]  B. Argall,et al.  Integration of Auditory and Visual Information about Objects in Superior Temporal Sulcus , 2004, Neuron.

[106]  G. Glover,et al.  Children's and adults’ neural bases of verbal and nonverbal ‘theory of mind’ , 2007, Neuropsychologia.

[107]  Satoshi Umeda,et al.  Gaze but not arrows: A dissociative impairment after right superior temporal gyrus damage , 2006, Neuropsychologia.

[108]  E. Rolls,et al.  Functional subdivisions of the temporal lobe neocortex , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[109]  Karl J. Friston,et al.  Assessing interactions among neuronal systems using functional neuroimaging , 2000, Neural Networks.

[110]  D. Perrett,et al.  Integration of form and motion in the anterior superior temporal polysensory area (STPa) of the macaque monkey. , 1996, Journal of neurophysiology.

[111]  Leslie G. Ungerleider,et al.  The Effect of Face Inversion on Activity in Human Neural Systems for Face and Object Perception , 1999, Neuron.

[112]  Lee M. Miller,et al.  Measuring interregional functional connectivity using coherence and partial coherence analyses of fMRI data , 2004, NeuroImage.