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

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.In rats, the rhythms of whisking and hippocampal theta become coherent precisely when rats approach and explore a texture; higher coherence enhances the identification of texture.Author Summary: Many regions of the mammalian brain exhibit oscillations in electrical activity. In rats, the 5–12 Hz theta rhythm is present in the hippocampus and in diverse areas of the cerebral cortex. What is the function of this rhythm? One proposal is that the exchange of information between two brain regions is facilitated whenever their respective oscillations are coherent. To test this idea, we ask whether theta oscillation in the hippocampus, a crucial memory structure located deep in the brain, is coherent with the rat’s rhythm of moving its whiskers and sensing the physical environment with them. We acquired hippocampal local field potentials (LFP)—extracellular voltage fluctuations within a small volume—while rats classified textures using cyclical whisker motion (“whisking”). At the moment of texture palpation, coherence between whisking and hippocampal theta oscillations increased by nearly 50%. At the same time, neuronal firing in sensory cortex became more phase-locked to the hippocampal theta oscillations. Rats identified the texture more rapidly and with lower error likelihood on trials characterized by an increase in hippocampal theta-whisking coherence during texture palpation. These results suggest that, as rats collect touch signals, enhanced coherence between the whisking rhythm, sensory cortex, and hippocampal LFP facilitates the integration of sensory information into memory and decision-making centers in the brain.