MIT HST 722J - Multisensory contributions to low-level, unisensory processing (5 pages)

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Multisensory contributions to low-level, unisensory processing



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Multisensory contributions to low level unisensory processing Charles E Schroeder and John Foxe Neurobiologists have traditionally assumed that multisensory integration is a higher order process that occurs after sensory signals have undergone extensive processing through a hierarchy of unisensory subcortical and cortical regions Recent findings however question this assumption Studies in humans nonhuman primates and other species demonstrate multisensory convergence in low level cortical structures that were generally believed to be unisensory in function In addition to enriching current models of multisensory processing and perceptual functions these new findings require a revision in our thinking about unisensory processing in low level cortical areas Addresses Cognitive Neuroscience and Schizophrenia Program The Nathan Kline Institute for Psychiatric Research 140 Old Orangeburg Rd Orangeburg NY 10962 and Program in Cognitive Neuroscience Department of Psychology The City College of the City University of New York North Academic Complex 138th Street and Convent Avenue New York NY 10031 USA Corresponding author Schroeder Charles E schrod nki rfmh org Current Opinion in Neurobiology 2005 15 454 458 This review comes from a themed issue on Sensory systems Edited by David Julius and Andrew King Available online 12th July 2005 0959 4388 see front matter 2005 Elsevier Ltd All rights reserved DOI 10 1016 j conb 2005 06 008 Introduction Recent studies in both monkey and human subjects have provided evidence for multisensory convergence at lowlevel putatively unisensory stages of the sensory cortical pathways 1 10 11 For example somatosensory responses can be observed in auditory belt cortical regions i e at the second level of auditory processing 4 and eye position input modulates auditory responses even at the primary cortical A1 level 12 13 Parallel findings have emerged in carnivores 12 14 Most dramatically two laboratories 15 16 have shown anatomical interconnections between low level visual and low level auditory areas which include the primary cortices V1 and A1 and two others have shown that eye position can affect the gain of auditory responses in A1 17 18 Recent reviews 9 19 20 have highlighted the fact that low level early multisensory convergence is paradoxical from a hierarchCurrent Opinion in Neurobiology 2005 15 454 458 ical sensory perspective and its functions are not yet clear This review focuses on low level multisensory convergence in the primate auditory system First we review the neurophysiological evidence in this area Second we discuss the potential anatomical sources of non auditory input and the types of projections used i e feedforward feedback lateral Finally we consider the functional implications of early multisensory integration in the context of the hierarchical model of auditory processing To avoid confusion we will use the term low level to refer to the anatomical stage at which a multisensory process is observed reserving the term early for reference to the time domain Visual and somatosensory responses in auditory cortex Studies using event related potentials ERPs in humans have demonstrated short latency audio visual 3 7 and audio somatosensory 21 22 interactions and have raised the possibility that these interactions occur in auditory cortices of the superior temporal plane Localization of multisensory interactions within the superior temporal plane is independently supported by findings from other brain imaging techniques that have better anatomical resolution including magnetoencephalography MEG 1 23 24 and functional magnetic resonance imaging fMRI 11 25 Intracranial recordings in several macaque species directly confirm multisensory convergence in auditory cortex 4 5 8 26 showing somatosensory and visual inputs in regions posterior to A1 The initial report of non auditory inputs 4 used multi electrode recordings in awake monkeys to show that somatosensory responses triggered by electrical stimulation of the median nerve have approximately the same latency as co located auditory responses and have a similar although not identical feedforward laminar profile That is the response begins in Lamina 4 and is followed by responses in the supra and infragranular laminae 27 The laminar profile of these inputs contrasts strongly with that of nearby visual inputs 5 27 These inputs have a feedback profile in that activity begins outside of Lamina 4 typically in the supragranular laminae and then spreads to Lamina 4 27 In addition a study 8 used microelectrode recordings in anesthetized monkeys to confirm that convergence occurs at the single neuron level 12 13 and showed that although cutaneous proprioceptive and vibratory inputs are present the dominant specific type of input is a cutaneous representation biased toward the skin surfaces of the head and neck www sciencedirect com Multisensory contributions to low level unisensory processing Schroeder and Foxe 455 Corresponding studies of specific visual properties have not yet been conducted although other studies e g 11 25 predict strong motion sensitivity These results fit into a complex of earlier findings on somatosensory inputs into the region of posterior auditory cortex in macaque monkeys Leinonen et al 28 reported auditory somatosensory co representation in Area Tpt the parabelt region occupying the posterior most portion of the superior temporal plane in macaque monkeys Also in macaques Robinson and Burton 29 described a body map in a medial retro insular RI region of the superior temporal plane in a location just medial to the caudomedial CM belt region of auditory cortex our ongoing studies P Lakatos and CE Schroeder unpublished show that RI receives auditory inputs Subsequently Krubitzer et al 30 suggested the existence of one or more body surface maps in a region they referred to as ventral somatosensory area VS which adjoins the medial edge foot representation of parietal operculum areas S2 and PV and extends out over the surface of the posterior superior temporal plane A portion of VS probably corresponds with the RI of Robinson and Burton 31 In any case in macaques the somatosensory region extending over the caudal superior temporal plane apparently corresponds to Areas CM MM and RI and possibly also to the caudo lateral CL belt area in addition to Area Tpt Anatomical mechanisms of multisensory convergence in auditory cortex In considering possible sources of somatosensory input to


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