Whisker stimulation reinforces a resting-state network in the barrel cortex: Nested oscillations and avalanches

Abstract The cerebral cortex operates in a state of restless activity, even in the absence of external stimuli. Collective neuronal activities, such as neural avalanches and synchronized oscillations, are also found under rest conditions, and these features have been suggested to support sensory processing, brain readiness for rapid responses, and computational efficiency. The rat barrel cortex and thalamus circuit, with its somatotopic organization for processing sensory inputs from the whiskers, provides a powerful system to explore such interplay. To characterize these resting state circuits, we perform simultaneous multi-electrode recordings in rats’ barrel cortex and thalamus. During spontaneous activity, oscillations with frequencies centered around 11 Hz are detected concomitantly with slow oscillations below 4 Hz, as well as power-law distributed avalanches. The phase of the lower-frequency oscillation appears to modulate the higher-frequency amplitude, and it has a role in gating avalanche occurrences. We then record neural activity during controlled whisker movements and observe that the 11 Hz barrel circuit active at rest is indeed the one involved in response to whisker stimulation. We finally show how a thalamic-driven firing-rate model can describe the entire phenomenology observed at resting state and predict the response of the barrel cortex to controlled whisker movement, suggesting that the same intrinsic dynamics underlying resting-state activity also shape sensory responses. Author Summary The brain is active even in the absence of external stimuli, generating complex patterns of activity that are thought to prepare it for processing incoming information. Two prominent features of this spontaneous activity are rhythmic oscillations and neuronal avalanches—bursts of activity that span a wide range of sizes and durations. However, how these patterns relate to actual sensory processing remains unclear. In this study, we investigated the rat barrel cortex, a well-characterized system for processing tactile information from whiskers. By combining electrophysiological recordings and computational modeling, we found that specific transient oscillations centered around 11 Hz are present during rest and become significantly stronger when the whiskers are stimulated. At the same time, spontaneous activity displays a rich dynamical regime with neuronal avalanches, whose timing is modulated by slower brain rhythms. Importantly, we show that a simple thalamus-driven computational model can reproduce these observations. We thus provide a minimal yet powerful model that suggests that the same rich, intrinsic dynamics underlying resting-state activity also shape sensory responses. Our results support the idea that spontaneous brain activity is not idle, but instead reflects an organized dynamical regime that facilitates efficient processing of sensory inputs.