Somatosensory and multisensory properties of the medial bank of the ferret rostral suprasylvian sulcus

In ferret cortex, the rostral portion of the suprasylvian sulcus separates primary somatosensory cortex (SI) from the anterior auditory fields. The boundary of the SI extends to this sulcus, but the adjoining medial sulcal bank has been described as “unresponsive.” Given its location between the representations of two different sensory modalities, it seems possible that the medial bank of the rostral suprasylvian sulcus (MRSS) might be multisensory in nature and contains neurons responsive to stimuli not examined by previous studies. The aim of this investigation was to determine if the MRSS contained tactile, auditory and/or multisensory neurons and to evaluate if its anatomical connections were consistent with these properties. The MRSS was found to be primarily responsive to low-threshold cutaneous stimulation, with regions of the head, neck and upper trunk represented somatotopically that were primarily connected with the SI face representation. Unlike the adjoining SI, the MRSS exhibited a different cytoarchitecture, its cutaneous representation was largely bilateral, and it contained a mixture of somatosensory, auditory and multisensory neurons. Despite the presence of multisensory neurons, however, auditory inputs exerted only modest effects on tactile processing in MRSS neurons and showed no influence on the averaged population response. These results identify the MRSS as a distinct, higher order somatosensory region as well as demonstrate that an area containing multisensory neurons may not necessarily exhibit activity indicative of multisensory processing at the population level.

[1]  M. Alex Meredith,et al.  Crossmodal projections from somatosensory area SIV to the auditory field of the anterior ectosylvian sulcus (FAES) in Cat: further evidence for subthreshold forms of multisensory processing , 2006, Experimental Brain Research.

[2]  H. R. Clemo,et al.  Organization of a fourth somatosensory area of cortex in cat. , 1983, Journal of neurophysiology.

[3]  Leslie P. Keniston,et al.  Subthreshold auditory inputs to extrastriate visual neurons are responsive to parametric changes in stimulus quality: Sensory-specific versus non-specific coding , 2008, Brain Research.

[4]  M. Carreras,et al.  Functional properties of neurons of the anterior ectosylvian gyrus of the cat. , 1963, Journal of neurophysiology.

[5]  J. Rauschecker,et al.  Centrifugal organization of direction preferences in the cat's lateral suprasylvian visual cortex and its relation to flow field processing , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  L. Krubitzer,et al.  Multisensory plasticity in congenitally deaf mice: How are cortical areas functionally specified? , 2006, Neuroscience.

[7]  Barry E Stein,et al.  Visual deprivation alters the development of cortical multisensory integration. , 2007, Journal of neurophysiology.

[8]  S. Shamma,et al.  Comparison of responses in the anterior and primary auditory fields of the ferret cortex. , 1995, Journal of neurophysiology.

[9]  A. L. Berman Interaction of cortical responses to somatic and auditory stimuli in anterior ectosylvian gyrus of cat. , 1961, Journal of neurophysiology.

[10]  A John Van Opstal,et al.  Crossmodal integration in the primate superior colliculus underlying the preparation and initiation of saccadic eye movements. , 2005, Journal of neurophysiology.

[11]  Brian L Allman,et al.  Do cross-modal projections always result in multisensory integration? , 2008, Cerebral cortex.

[12]  R. Dykes,et al.  Cytoarchitecture of the ferret suprasylvian gyrus correlated with areas containing multiunit responses elicited by stimulation of the face. , 1993, Somatosensory & motor research.

[13]  L. Arckens,et al.  Neurofilament protein: A selective marker for the architectonic parcellation of the visual cortex in adult cat brain , 2001, The Journal of comparative neurology.

[14]  C. Avendaño,et al.  Organization of the association cortical afferent connections of area 5: A retrograde tracer study in the cat , 1988, The Journal of comparative neurology.

[15]  Jeffery A Winer,et al.  A multisensory zone in rat parietotemporal cortex: Intra‐ and extracellular physiology and thalamocortical connections , 2003, The Journal of comparative neurology.

[16]  R. Dykes,et al.  Electrophysiological examination of the representation of the face in the suprasylvian gyrus of the ferret: a correlative study with cytoarchitecture. , 1993, Somatosensory & motor research.

[17]  R. Dykes,et al.  Somatotopic projections of mystacial vibrissae on cerebral cortex of cats. , 1977, Journal of neurophysiology.

[18]  Giorgio M Innocenti,et al.  Areal organization of the posterior parietal cortex of the ferret (Mustela putorius). , 2002, Cerebral cortex.

[19]  Brian L Allman,et al.  Multisensory processing in "unimodal" neurons: cross-modal subthreshold auditory effects in cat extrastriate visual cortex. , 2007, Journal of neurophysiology.

[20]  A. Reiner,et al.  Biotinylated dextran amine as an anterograde tracer for single- and double-labeling studies , 1992, Journal of Neuroscience Methods.

[21]  B. Allman,et al.  Auditory projections to extrastriate visual cortex: connectional basis for multisensory processing in ‘unimodal’ visual neurons , 2008, Experimental Brain Research.

[22]  L. Palmer,et al.  The retinotopic organization of lateral suprasylvian visual areas in the cat , 1978, The Journal of comparative neurology.

[23]  H. R. Clemo,et al.  Cross-modal circuitry between auditory and somatosensory areas of the cat anterior ectosylvian sulcal cortex: a 'new' inhibitory form of multisensory convergence. , 2004, Cerebral cortex.

[24]  Dr. C. J. Heath,et al.  The Anatomical Organization of the Suprasylvian Gyrus of the Cat , 1971, Advances in Anatomy, Embryology and Cell Biology.

[25]  S. Juliano,et al.  Organization of the forepaw representation in ferret somatosensory cortex. , 1998, Somatosensory & motor research.

[26]  C. Woolsey,et al.  Contralateral, ipsilateral, and bilateral representation of cutaneous receptors in somatic areas I and II of the cerebral cortex of pig, sheep, and other mammals. , 1946, Surgery.

[27]  R. Reale,et al.  Tonotopic organization in auditory cortex of the cat , 1980, The Journal of comparative neurology.

[28]  A. L. Berman Overlap of somatic and auditory cortical response fields in anterior ectosylvian gyrus of cat. , 1961, Journal of neurophysiology.

[29]  M. Meredith,et al.  Multiple sensory afferents to ferret pseudosylvian sulcal cortex , 2004, Neuroreport.

[30]  S P Wise,et al.  Cytoarchitecture and thalamic connectivity of third somatosensory area of cat cerebral cortex. , 1978, Journal of neurophysiology.

[31]  D J Felleman,et al.  Somatotopic organization of the lateral sulcus of owl monkeys: Area 3b, s‐II, and a ventral somatosensory area , 1989, The Journal of comparative neurology.

[32]  I. Nelken,et al.  Functional organization of ferret auditory cortex. , 2005, Cerebral cortex.

[33]  J. Driver,et al.  Multisensory Interplay Reveals Crossmodal Influences on ‘Sensory-Specific’ Brain Regions, Neural Responses, and Judgments , 2008, Neuron.

[34]  M. Wallace,et al.  Superior colliculus neurons use distinct operational modes in the integration of multisensory stimuli. , 2005, Journal of neurophysiology.

[35]  D. Ferrington,et al.  Tactile neuron classes within second somatosensory area (SII) of cat cerebral cortex. , 1980, Journal of neurophysiology.

[36]  C. Robinson,et al.  Organization of somatosensory receptive fields in cortical areas 7b, retroinsula, postauditory and granular insula of M. fascicularis , 1980, The Journal of comparative neurology.

[37]  M. Wallace,et al.  A revised view of sensory cortical parcellation , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[38]  Brian L Allman,et al.  Subthreshold multisensory processing in cat auditory cortex , 2009, Neuroreport.

[39]  John C Middlebrooks,et al.  Spatial sensitivity in the dorsal zone (area DZ) of cat auditory cortex. , 2005, Journal of neurophysiology.

[40]  A. Graybiel Some fiber pathways related to the posterior thalamic region in the cat. , 1972, Brain, behavior and evolution.

[41]  Anterior ectosylvian cortical projections to the rostral suprasylvian multisensory zone in cat , 2003, Neuroreport.

[42]  C. J. Heath,et al.  An experimental study of ascending connections from the posterior group of thalamic nuclei in the cat , 1971, The Journal of comparative neurology.

[43]  H. R. Clemo,et al.  Sensory and multisensory representations within the cat rostral suprasylvian cortex , 2007, The Journal of comparative neurology.