The somatosensory barrel cortex controls the spindlethalamocortical oscillation by frequency locking

Abstract

The sleep spindle is a characteristic oscillation typically observed in NREM sleep and anesthesia. It is generated by a closed-loop thalamocortical circuit that is allegedly contributing to thalamocortical gating, sensory processing and memory consolidation. Yet, the circuit intricacy in terms of electrophysiological neuronal properties and connectivity has so far contributed to hinder a clear understanding of its regulation and function. In this study, we experimentally demonstrate that, when driven by the somatosensory cortex, the spindle circuit behaves as a macroscopic single-frequency self-sustained oscillator. We frequency-modulated cortical inputs to the thalamocortical spindle circuit by periodic microstimulation of the barrel cortex in the anesthetized rat. Cortical spindles exhibited synchronization by frequency locking and not resonance, displaying a characteristic Arnold tongue, a hallmark of the self-sustained oscillator. With a rate model of the barrel cortex-thalamus circuit reproducing the oscillator behavior we show that frequency-locking can govern synchronization under whisking. Significance statementTemporal coordination across neurons (neural synchronization) is believed to be a fundamental mechanism underlying brain information processing. Neural synchornization generates oscillatory signals such as waxing and waning, approximately 10 Hz oscillations occurring during sleep and anaesthesia and known as brain spindles. Spindles are generated by a closed-loop circuit between thalamus and cortex but their function remains unknown. We demonstrate that, similarly to a methronome that adjusts its frequency to the one of an external forcing oscillator, the spindle circuit is controlled by the sensory cortex according to a frequency-locking mechanism. We suggest that frequency-locking within the thalmocortical circuitry represents a flexible frequency-adjustable mechanism tuning the processing of sensory inputs by neural synchronization.