Multimodal interactions between proprioceptive and cutaneous signals in primary somatosensory cortex
Identifieur interne : 000445 ( Pmc/Checkpoint ); précédent : 000444; suivant : 000446Multimodal interactions between proprioceptive and cutaneous signals in primary somatosensory cortex
Auteurs : Sung Soo Kim [États-Unis] ; Manuel Gomez-Ramirez [États-Unis] ; Pramodsingh H. Thakur [États-Unis] ; Steven S. Hsiao [États-Unis]Source :
- Neuron [ 0896-6273 ] ; 2015.
Abstract
The classical view of somatosensory processing holds that proprioceptive and cutaneous inputs are conveyed to cortex through segregated channels, initially synapsing in modality-specific areas 3a (proprioception) and 3b (cutaneous) of primary somatosensory cortex (SI). These areas relay their signals to areas 1 and 2 where multimodal convergence first emerges. However, proprioceptive and cutaneous maps have traditionally been characterized using unreliable stimulation tools. Here, we employed a mechanical stimulator that reliably positioned animals' hands in different postures and presented tactile stimuli with superb precision. Single-unit recordings in SI revealed that most neurons responded to cutaneous and proprioceptive stimuli, including cells in areas 3a and 3b. Multimodal responses were characterized by linear and nonlinear effects that emerged during early (∼20ms) and latter (>100ms) stages of stimulus processing, respectively. These data are incompatible with the modality specificity model in SI, and provide evidence for distinct mechanisms of multimodal processing in the somatosensory system.
Url:
DOI: 10.1016/j.neuron.2015.03.020
PubMed: 25864632
PubMed Central: 4409561
Affiliations:
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<front><div type="abstract" xml:lang="en"><p id="P1">The classical view of somatosensory processing holds that proprioceptive and cutaneous inputs are conveyed to cortex through segregated channels, initially synapsing in modality-specific areas 3a (proprioception) and 3b (cutaneous) of primary somatosensory cortex (SI). These areas relay their signals to areas 1 and 2 where multimodal convergence first emerges. However, proprioceptive and cutaneous maps have traditionally been characterized using unreliable stimulation tools. Here, we employed a mechanical stimulator that reliably positioned animals' hands in different postures and presented tactile stimuli with superb precision. Single-unit recordings in SI revealed that most neurons responded to cutaneous and proprioceptive stimuli, including cells in areas 3a and 3b. Multimodal responses were characterized by linear and nonlinear effects that emerged during early (∼20ms) and latter (>100ms) stages of stimulus processing, respectively. These data are incompatible with the modality specificity model in SI, and provide evidence for distinct mechanisms of multimodal processing in the somatosensory system.</p>
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<article-categories><subj-group subj-group-type="heading"><subject>Article</subject>
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<title-group><article-title>Multimodal interactions between proprioceptive and cutaneous signals in primary somatosensory cortex</article-title>
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<contrib-group><contrib contrib-type="author"><name><surname>Kim</surname>
<given-names>Sung Soo</given-names>
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<xref ref-type="aff" rid="A1">1</xref>
<xref ref-type="aff" rid="A2">2</xref>
<xref ref-type="aff" rid="A4">4</xref>
<xref rid="FN1" ref-type="author-notes">#</xref>
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<contrib contrib-type="author"><name><surname>Gomez-Ramirez</surname>
<given-names>Manuel</given-names>
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<contrib contrib-type="author"><name><surname>Thakur</surname>
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<contrib contrib-type="author"><name><surname>Hsiao</surname>
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<aff id="A1"><label>1</label>
The Zanvyl Krieger Mind/Brain Institute, The Johns Hopkins University, Baltimore, MD 21218</aff>
<aff id="A2"><label>2</label>
The Solomon H Snyder Department of Neuroscience, The Johns Hopkins School of Medicine, Baltimore, MD 21218</aff>
<aff id="A3"><label>3</label>
Department of Biomedical Engineering, The Johns Hopkins University, Baltimore, MD 21218</aff>
<aff id="A4"><label>4</label>
Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, Virginia, 20147</aff>
<author-notes><corresp id="FN1"><label>#</label>
Correspondences: <bold>Sung Soo Kim, Ph.D</bold>
, Janelia Research Campus, Howard Hughes Medical Institute, 19700 Helix Drive, Ashburn, VA 20147, <email>sungsoo@janelia.hhmi.org</email>
; <bold>Manuel Gomez-Ramirez, Ph.D</bold>
, Zanvyl Krieger Mind/Brain Institute, 338 Krieger Hall, The Johns Hopkins University, 3400 N. Charles St., Baltimore, MD 21218, Telephone: 410-516-6412, Fax: 410-516-8648, <email>gomezramirezm@jhu.edu</email>
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<pub-date pub-type="pmc-release"><day>22</day>
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<pmc-comment>elocation-id from pubmed: 10.1016/j.neuron.2015.03.020</pmc-comment>
<permissions><copyright-statement>© 2015 Published by Elsevier Inc.</copyright-statement>
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<abstract><p id="P1">The classical view of somatosensory processing holds that proprioceptive and cutaneous inputs are conveyed to cortex through segregated channels, initially synapsing in modality-specific areas 3a (proprioception) and 3b (cutaneous) of primary somatosensory cortex (SI). These areas relay their signals to areas 1 and 2 where multimodal convergence first emerges. However, proprioceptive and cutaneous maps have traditionally been characterized using unreliable stimulation tools. Here, we employed a mechanical stimulator that reliably positioned animals' hands in different postures and presented tactile stimuli with superb precision. Single-unit recordings in SI revealed that most neurons responded to cutaneous and proprioceptive stimuli, including cells in areas 3a and 3b. Multimodal responses were characterized by linear and nonlinear effects that emerged during early (∼20ms) and latter (>100ms) stages of stimulus processing, respectively. These data are incompatible with the modality specificity model in SI, and provide evidence for distinct mechanisms of multimodal processing in the somatosensory system.</p>
</abstract>
<kwd-group><kwd>convergence</kwd>
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<kwd>macaca mulatta</kwd>
<kwd>additive</kwd>
<kwd>non-additive</kwd>
<kwd>local features</kwd>
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<name sortKey="Thakur, Pramodsingh H" sort="Thakur, Pramodsingh H" uniqKey="Thakur P" first="Pramodsingh H." last="Thakur">Pramodsingh H. Thakur</name>
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