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Processing of tactile information by the hippocampus

Identifieur interne : 002433 ( Pmc/Checkpoint ); précédent : 002432; suivant : 002434

Processing of tactile information by the hippocampus

Auteurs : Antonio Pereira [Brésil] ; Sidarta Ribeiro [Brésil] ; Michael Wiest ; Leonardo C. Moore ; Janaina Pantoja ; Shih-Chieh Lin ; Miguel A. L. Nicolelis [Brésil, États-Unis, Suisse]

Source :

RBID : PMC:2084335

Abstract

The ability to detect unusual events occurring in the environment is essential for survival. Several studies have pointed to the hippocampus as a key brain structure in novelty detection, a claim substantiated by its wide access to sensory information through the entorhinal cortex and also distinct aspects of its intrinsic circuitry. Novelty detection is implemented by an associative match–mismatch algorithm involving the CA1 and CA3 hippocampal subfields that compares the stream of sensory inputs received by CA1 to the stored representation of spatiotemporal sequences in CA3. In some rodents, including the rat, the highly sensitive facial whiskers are responsible for providing accurate tactile information about nearby objects. Surprisingly, however, not much is known about how inputs from the whiskers reach CA1 and how they are processed therein. Using concurrent multielectrode neuronal recordings and chemical inactivation in behaving rats, we show that trigeminal inputs from the whiskers reach the CA1 region through thalamic and cortical relays associated with discriminative touch. Ensembles of hippocampal neurons also carry precise information about stimulus identity when recorded during performance in an aperture-discrimination task using the whiskers. We also found broad similarities between tactile responses of trigeminal stations and the hippocampus during different vigilance states (wake and sleep). Taken together, our results show that tactile information associated with fine whisker discrimination is readily available to the hippocampus for dynamic updating of spatial maps.


Url:
DOI: 10.1073/pnas.0708611104
PubMed: 17989221
PubMed Central: 2084335


Affiliations:


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PMC:2084335

Le document en format XML

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<p>The ability to detect unusual events occurring in the environment is essential for survival. Several studies have pointed to the hippocampus as a key brain structure in novelty detection, a claim substantiated by its wide access to sensory information through the entorhinal cortex and also distinct aspects of its intrinsic circuitry. Novelty detection is implemented by an associative match–mismatch algorithm involving the CA1 and CA3 hippocampal subfields that compares the stream of sensory inputs received by CA1 to the stored representation of spatiotemporal sequences in CA3. In some rodents, including the rat, the highly sensitive facial whiskers are responsible for providing accurate tactile information about nearby objects. Surprisingly, however, not much is known about how inputs from the whiskers reach CA1 and how they are processed therein. Using concurrent multielectrode neuronal recordings and chemical inactivation in behaving rats, we show that trigeminal inputs from the whiskers reach the CA1 region through thalamic and cortical relays associated with discriminative touch. Ensembles of hippocampal neurons also carry precise information about stimulus identity when recorded during performance in an aperture-discrimination task using the whiskers. We also found broad similarities between tactile responses of trigeminal stations and the hippocampus during different vigilance states (wake and sleep). Taken together, our results show that tactile information associated with fine whisker discrimination is readily available to the hippocampus for dynamic updating of spatial maps.</p>
</div>
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<article-id pub-id-type="pmc">2084335</article-id>
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<article-title>Processing of tactile information by the hippocampus</article-title>
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<name>
<surname>Pereira</surname>
<given-names>Antonio</given-names>
</name>
<xref ref-type="aff" rid="aff1">*</xref>
<xref ref-type="aff" rid="aff2">
<sup></sup>
</xref>
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<name>
<surname>Ribeiro</surname>
<given-names>Sidarta</given-names>
</name>
<xref ref-type="aff" rid="aff6">
<sup></sup>
</xref>
<xref ref-type="aff" rid="aff7">
<sup>§</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Wiest</surname>
<given-names>Michael</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup></sup>
</xref>
<xref ref-type="aff" rid="aff3">
<sup></sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Moore</surname>
<given-names>Leonardo C.</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup></sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Pantoja</surname>
<given-names>Janaina</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup></sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Lin</surname>
<given-names>Shih-Chieh</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup></sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Nicolelis</surname>
<given-names>Miguel A. L.</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup></sup>
</xref>
<xref ref-type="aff" rid="aff6">
<sup></sup>
</xref>
<xref ref-type="aff" rid="aff3">
<sup></sup>
</xref>
<xref ref-type="aff" rid="aff5">**</xref>
<xref ref-type="aff" rid="aff4">
<sup></sup>
</xref>
<xref ref-type="aff" rid="aff8">
<sup>††</sup>
</xref>
<xref ref-type="corresp" rid="cor1">
<sup>‡‡</sup>
</xref>
</contrib>
<aff id="aff1">*Departamento de Fisiologia, Universidade Federal do Pará, PA 66075-900, Belém, Brazil;</aff>
<aff id="aff2">
<sup></sup>
Department of Neurobiology,</aff>
<aff id="aff3">
<sup></sup>
Center for Neuroengineering,</aff>
<aff id="aff4">
<sup></sup>
Department of Biomedical Engineering, and</aff>
<aff id="aff5">**Department of Cognitive and Brain Sciences, Duke University, Durham, NC 27710;</aff>
<aff id="aff6">
<sup></sup>
Edmond and Lily Safra International Institute of Neuroscience of Natal, RN 59066-060, Natal, Brazil;</aff>
<aff id="aff7">
<sup>§</sup>
Departamento de Fisiologia, Universidade Federal do Rio Grande do Norte, RN 59072-970, Natal, Brazil; and</aff>
<aff id="aff8">
<sup>††</sup>
Laboratory of Neural Ensemble Technology, École Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland</aff>
</contrib-group>
<author-notes>
<corresp id="cor1">
<sup>‡‡</sup>
To whom correspondence should be addressed. E-mail:
<email>nicoleli@neuro.duke.edu</email>
</corresp>
<fn fn-type="com">
<p>Communicated by Jon H. Kaas, Vanderbilt University, Nashville, TN, September 11, 2007</p>
</fn>
<fn fn-type="con">
<p>Author contributions: A.P. and S.R. designed research; A.P., M.W., L.C.M., and J.P. performed research; A.P., M.W., S.-C.L., and M.A.L.N. contributed new reagents/analytic tools; A.P. and M.W. analyzed data; and A.P., S.R., and M.A.L.N. wrote the paper.</p>
</fn>
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<month>11</month>
<year>2007</year>
</pub-date>
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<year>2007</year>
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<month>6</month>
<year>2007</year>
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<abstract>
<p>The ability to detect unusual events occurring in the environment is essential for survival. Several studies have pointed to the hippocampus as a key brain structure in novelty detection, a claim substantiated by its wide access to sensory information through the entorhinal cortex and also distinct aspects of its intrinsic circuitry. Novelty detection is implemented by an associative match–mismatch algorithm involving the CA1 and CA3 hippocampal subfields that compares the stream of sensory inputs received by CA1 to the stored representation of spatiotemporal sequences in CA3. In some rodents, including the rat, the highly sensitive facial whiskers are responsible for providing accurate tactile information about nearby objects. Surprisingly, however, not much is known about how inputs from the whiskers reach CA1 and how they are processed therein. Using concurrent multielectrode neuronal recordings and chemical inactivation in behaving rats, we show that trigeminal inputs from the whiskers reach the CA1 region through thalamic and cortical relays associated with discriminative touch. Ensembles of hippocampal neurons also carry precise information about stimulus identity when recorded during performance in an aperture-discrimination task using the whiskers. We also found broad similarities between tactile responses of trigeminal stations and the hippocampus during different vigilance states (wake and sleep). Taken together, our results show that tactile information associated with fine whisker discrimination is readily available to the hippocampus for dynamic updating of spatial maps.</p>
</abstract>
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