Processing of tactile information by the hippocampus

*Departamento de Fisiologia, Universidade Federal do Pará, PA 66075-900, Belém, Brazil;
^†Department of Neurobiology,
^¶Center for Neuroengineering,
^‖Department of Biomedical Engineering, and
**Department of Cognitive and Brain Sciences, Duke University, Durham, NC 27710;
^‡Edmond and Lily Safra International Institute of Neuroscience of Natal, RN 59066-060, Natal, Brazil;
^§Departamento de Fisiologia, Universidade Federal do Rio Grande do Norte, RN 59072-970, Natal, Brazil; and
^††Laboratory of Neural Ensemble Technology, École Polytechnique Fédérale de Lausanne, CH-1015 Lausanne, Switzerland

Communicated by Jon H. Kaas, Vanderbilt University, Nashville, TN, September 11, 2007 (received for review June 29, 2007)

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.

Footnotes

^‡‡To whom correspondence should be addressed. E-mail: nicoleli{at}neuro.duke.edu
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.
The authors declare no conflict of interest.
Abbreviations:

IO,

infraorbital;

LFP,

local field potential;

LVQ,

learning vector quantization;

QWK,

quiet waking;

REM,

rapid eye movement;

S1,

primary somatosensory cortex;

SWS,

slow-wave sleep;

VPM,

ventral posteromedial nucleus.
Freely available online through the PNAS open access option.