Functional topography of working memory for face or voice identity

We used functional magnetic resonance imaging (fMRI) to investigate whether the neural systems for nonspatial visual and auditory working memory exhibits a functional dissociation. The subjects performed a delayed recognition task for previously unfamiliar faces and voices and an audiovisual sensorimotor control task. During the initial sample and subsequent test stimulus presentations, activation was greater for the face than for the voice identity task bilaterally in the occipitotemporal cortex and, conversely, greater for voices than for faces bilaterally in the superior temporal sulcus/gyrus (STS/STG). Ventral prefrontal regions were activated by both memory delays in comparison with the control delays, and there was no significant difference in direct voxelwise comparisons between the tasks. However, further analyses showed that there was a subtle difference in the functional topography for two delay types within the ventral prefrontal cortex. Face delays preferentially activate the dorsal part of the ventral prefrontal cortex (BA 44/45) while voice delays preferentially activate the inferior part (BA 45/47), indicating a ventral/dorsal auditory/visual topography within the ventral prefrontal cortex. The results confirm that there is a modality-specific attentional modulation of activity in visual and auditory sensory areas during stimulus presentation. Moreover, within the nonspatial information-type domain, there is a subtle across-modality dissociation within the ventral prefrontal cortex during working memory maintenance of faces and voices.

[1]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

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

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

[4]  Andy C. H. Lee,et al.  “Pray or Prey?” Dissociation of Semantic Memory Retrieval from Episodic Memory Processes Using Positron Emission Tomography and a Novel Homophone Task , 2002, NeuroImage.

[5]  Edward E. Smith,et al.  PET Evidence for an Amodal Verbal Working Memory System , 1996, NeuroImage.

[6]  Leslie G. Ungerleider Two cortical visual systems , 1982 .

[7]  Scott T. Grafton,et al.  Automated image registration: I. General methods and intrasubject, intramodality validation. , 1998, Journal of computer assisted tomography.

[8]  Leslie G. Ungerleider,et al.  ‘What’ and ‘where’ in the human brain , 1994, Current Opinion in Neurobiology.

[9]  Terri Gullickson Human Brain Anatomy in Computerized Images. , 1995 .

[10]  M. Hallett,et al.  Neural correlates of cross-modal binding , 2003, Nature Neuroscience.

[11]  J J Pekar,et al.  Dissociation of the neural systems for working memory maintenance of verbal and nonspatial visual information , 2001, Cognitive, affective & behavioral neuroscience.

[12]  Tyrone D. Cannon,et al.  Maintenance and Manipulation in Spatial Working Memory: Dissociations in the Prefrontal Cortex , 2002, NeuroImage.

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

[14]  M. Azuma,et al.  Properties and distribution of auditory neurons in the dorsolateral prefrontal cortex of the alert monkey , 1984, Brain Research.

[15]  P. Goldman-Rakic,et al.  An auditory domain in primate prefrontal cortex , 2002, Nature Neuroscience.

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

[17]  Leslie G. Ungerleider,et al.  The role of prefrontal cortex in working memory: examining the contents of consciousness. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[18]  W. Singer,et al.  Distributed cortical systems in visual short-term memory revealed by event-related functional magnetic resonance imaging. , 2002, Cerebral cortex.

[19]  Jonathan D. Cohen,et al.  Working Memory for Letters, Shapes, and Locations: fMRI Evidence against Stimulus-Based Regional Organization in Human Prefrontal Cortex , 2000, NeuroImage.

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

[21]  J. Haxby,et al.  fMRI study of face perception and memory using random stimulus sequences. , 1998, Journal of neurophysiology.

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

[23]  Leslie G. Ungerleider,et al.  An area specialized for spatial working memory in human frontal cortex. , 1998, Science.

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

[25]  D. Yves von Cramon,et al.  The functional neuroanatomy of human working memory revisited Evidence from 3-T fMRI studies using classical domain-specific interference tasks , 2003, NeuroImage.

[27]  K. Zilles,et al.  The neural correlates of person familiarity. A functional magnetic resonance imaging study with clinical implications. , 2001, Brain : a journal of neurology.

[28]  V Menon,et al.  Modality effects in verbal working memory: differential prefrontal and parietal responses to auditory and visual stimuli , 2004, NeuroImage.

[29]  Leslie G. Ungerleider,et al.  Object and spatial visual working memory activate separate neural systems in human cortex. , 1996, Cerebral cortex.

[30]  Joseph B. Sala,et al.  Functional topography of a distributed neural system for spatial and nonspatial information maintenance in working memory , 2003, Neuropsychologia.

[31]  P. Goldman-Rakic,et al.  Segregation of working memory functions within the dorsolateral prefrontal cortex , 2000, Experimental Brain Research.

[32]  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.

[33]  Edward E. Smith,et al.  Dissociation of Storage and Rehearsal in Verbal Working Memory: Evidence From Positron Emission Tomography , 1996 .

[34]  T. Allison,et al.  Face-sensitive regions in human extrastriate cortex studied by functional MRI. , 1995, Journal of neurophysiology.

[35]  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.

[36]  Leslie G. Ungerleider,et al.  Transient and sustained activity in a distributed neural system for human working memory , 1997, Nature.

[37]  Leslie G. Ungerleider,et al.  The functional organization of human extrastriate cortex: a PET-rCBF study of selective attention to faces and locations , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  Joseph B. Sala,et al.  Dissociable functional cortical topographies for working memory maintenance of voice identity and location. , 2004, Cerebral cortex.

[39]  Edward E. Smith,et al.  Verbal Working Memory Load Affects Regional Brain Activation as Measured by PET , 1997, Journal of Cognitive Neuroscience.

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

[41]  J. Jonides,et al.  Storage and executive processes in the frontal lobes. , 1999, Science.

[42]  J. Sergent,et al.  Functional neuroanatomy of face and object processing. A positron emission tomography study. , 1992, Brain : a journal of neurology.

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

[44]  J. Haxby,et al.  Functional Magnetic Resonance Imaging of Human Visual Cortex during Face Matching: A Comparison with Positron Emission Tomography , 1996, NeuroImage.

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

[46]  R. Mansfield,et al.  Analysis of visual behavior , 1982 .