Dynamic coupling between whisking, barrel cortex, and hippocampus during texture discrimination: A role for slow rhythms

Increasing amounts of work have demonstrated that brain rhythms might constitute clocking mechanisms against which to coordinate sequences of neural firing; such rhythms may be essential to the coding operations performed by the local networks. The sequence of operations underlying a tactile discrimination task in rats requires the animal to integrate two streams of information, those coming from the environment and, from reference memory the rules that dictate the correct response. The current study is a follow up on the work which has described the hippocampal representation of the tactile guided task. We have used a well-established texture discrimination task, in which rats have to associate two stimuli with two different reward locations. We placed microelectrodes in primary somatosensory cortex and the CA1 region of hippocampus to perform recordings of spiking activity and local field potentials when the animal touched the discriminandum as well as when he was in a resting state. We also performed recording on an arena in which the animal moved freely and did not perform any task. Earlier work has demonstrated that tactile signals reach the hippocampus during texture discrimination, presumably through the somatosensory cortex. We predicted that neurons in the primary somatosensory cortex (S1) are entrained to the oscillatory theta rhythm that permeates the hippocampus. Our expectation is that such coherence could serve to increase the reliability of synaptic transmission, linking the acquisition of new sensory information with associative processes. We addressed the following issues: Is the timing of action potentials in S1 modulated by the ongoing hippocampal theta rhythm? If so, is the occurrence of this modulation aligned in time to the period in which the hippocampus acquires tactile signals? We also predicted that the 10-Hz whisking that characterizes the acquisition of texture information would be more strongly phase locked to theta rhythm than the whisking in the air that is not accompanied by any explicit tactile task. We speculate that such phase locking could be a means to synchronize sensory and hippocampal processing. The notion that the coordination between brain areas might be related to the rhythmic of sensorimotor cycles is particularly appealing. We have found that the firing of 18% of barrel cells was significantly modulated by hippocampal theta during the half-second period of active tactile discrimination. Importantly, we found that during periods of rest interleaved in the session, neurons significantly decreased the degree of phase-locking with respect to touch. We hypothesize that areas involved with motivational processes as basal ganglia could gate the entrainment during task related epochs. S1 neurons were classified as those excited by contact with the discriminandum, and those not excited by contact. The firing of both sorts of neurons was modulated by CA1 theta rhythm during exploration of the texture. However the theta phase to which they fired preferentially was opposite; contact-responsive neurons tended to fire in the upward phases of the cycle whereas contact non-responsive neurons tended to fire in the downward phase of the cycle suggesting that theta rhythm might have the function of temporally separating sensory cortical neurons according to their functional properties and the information they carry. By clustering touch-sensitive neurons to a certain time window and separating them from ‘non-informative’ neurons, theta rhythm could increase the efficiency not only of information tranfer to hippocampus but also the efficiency of information encoding/decoding. We also found phase and amplitude relationships between whisking and hippocampal theta during the goal-directed tactile task; the relationships disappear when the animal moves along an open arena, still actively whisking but not engaged in the texture discrimination task. We were able to show, for the first time to our knowledge, that CA1 theta rhythm can exert a behavioral state-dependent modulatory effect on sensory cortex. S1 neuron firing and whisking activity are entrained to hippocampal theta rhythm when the animal collects meaningful tactile information from the environment.