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Population dynamics of sensory adaptation in cortical circuits

Abstract

Our sensory systems are remarkably flexible, able to adjust and recalibrate as we move through environments composed of drastically different stimuli. This flexibility is achieved in part through sensory adaptation (SA), a process whereby brain circuits adjust neuronal activity based on the spatiotemporal context in which stimuli are encountered. Several functions have been proposed for SA, including the improvement of discrimination between stimuli, maximizing information transmission in the current sensory environment, and the reduction of metabolic costs. While SA has been extensively studied at the level of individual neurons on timescales of tens of milliseconds to a few seconds, little is known about SA over longer timescales or at the population level. Here, we investigate population-level SA in the barrel field of the mouse somatosensory cortex (S1BF), which processes whisker inputs, using in vivo 2-photon calcium imaging and Neuropixels recordings of excitatory neurons in awake mice. Amongst stimulus responsive (SR) neurons we found both adapting and facilitating neurons that decreased or increased their firing with repetitive whisker stimulation, respectively. We also discovered that population SA to one stimulus frequency does not necessarily generalize to a different frequency. Moreover, responses of individual neurons to repeated rounds of stimulation were strikingly heterogeneous and stochastic, such that their adapting or facilitating response profile to the same stimulus was not stable across tens of minutes. Such representational drift was particularly striking when recording longitudinally across several days, as SA response profiles of most SR neurons changed drastically from one day to the next. Remarkably, repeated exposure to a familiar stimulus paradoxically shifted the population away from strong adaptation and toward facilitation. Finally, we investigated SST interneurons as a candidate network mechanism underlying population SA, and our preliminary results suggest they may modulate the balance between adaptation and facilitation in S1BF. Together, our studies indicate that the SA profile of S1BF neurons is not a fixed property of neurons, but rather highly a dynamic feature that is shaped by sensory experience across days. These findings provide valuable insight into the complex dynamics of population SA in S1BF and will serve as an important reference for future mechanistic studies of population SA as well as interrogations of its potential alteration in neurological and psychiatric conditions.

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