Coherence between Rat Sensorimotor System and Hippocampus Is Enhanced during Tactile Discrimination

PLoS Biol. 2016 Feb 18;14(2):e1002384. doi: 10.1371/journal.pbio.1002384. eCollection 2016 Feb.

Abstract

Rhythms with time scales of multiple cycles per second permeate the mammalian brain, yet neuroscientists are not certain of their functional roles. One leading idea is that coherent oscillation between two brain regions facilitates the exchange of information between them. In rats, the hippocampus and the vibrissal sensorimotor system both are characterized by rhythmic oscillation in the theta range, 5-12 Hz. Previous work has been divided as to whether the two rhythms are independent or coherent. To resolve this question, we acquired three measures from rats--whisker motion, hippocampal local field potential (LFP), and barrel cortex unit firing--during a whisker-mediated texture discrimination task and during control conditions (not engaged in a whisker-mediated memory task). Compared to control conditions, the theta band of hippocampal LFP showed a marked increase in power as the rats approached and then palpated the texture. Phase synchronization between whisking and hippocampal LFP increased by almost 50% during approach and texture palpation. In addition, a greater proportion of barrel cortex neurons showed firing that was phase-locked to hippocampal theta while rats were engaged in the discrimination task. Consistent with a behavioral consequence of phase synchronization, the rats identified the texture more rapidly and with lower error likelihood on trials in which there was an increase in theta-whisking coherence at the moment of texture palpation. These results suggest that coherence between the whisking rhythm, barrel cortex firing, and hippocampal LFP is augmented selectively during epochs in which the rat collects sensory information and that such coherence enhances the efficiency of integration of stimulus information into memory and decision-making centers.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CA1 Region, Hippocampal / physiology*
  • Male
  • Rats, Wistar
  • Somatosensory Cortex / physiology*
  • Theta Rhythm*
  • Touch Perception / physiology*
  • Vibrissae / physiology*

Grant support

We acknowledge the financial support of the Human Frontier Science Program (http://www.hfsp.org; projects RG0041/2009-C and RG0015/2013), the European Research Council Advanced grant CONCEPT (http://erc.europa.eu; project 294498), European Community's Seventh Framework Programme project CORONET (http://cordis.europa.eu/fp7/ict/home_en.html; project 269459), and Italian MIUR grant HANDBOT (http://hubmiur.pubblica.istruzione.it/web/ricerca/home; project GA 280778). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.