An increase in spontaneous activity mediates visual habituation

Abstract

The cerebral cortex is spontaneously active, but the function of this ongoing activity remains unclear. One possibility is that spontaneous activity provides contextual information in cortical computations, replaying previously learned patterns of activity that conditions the cortex to respond more efficiently, based on past experience. To test this, we measured the response of neuronal populations in mouse primary visual cortex with chronic two-photon calcium imaging during a visual habituation to a specific oriented stimulus. We unexpectedly found that, during habituation, spontaneous activity increased in neurons across the full range of orientation selectivity, eventually matching that of evoked levels. The increase in spontaneous activity strongly correlated with the degree of habituation. In fact, boosting spontaneous activity with two-photon optogenetic stimulation to the levels of stimulus-evoked activity induced habituation in naive animals. Our study shows that cortical spontaneous activity is causally linked to habituation, which unfolds by minimizing the difference between spontaneous and stimulus-evoked activity levels, rendering the cortex less responsive. We also show how manipulating spontaneous activity can accelerate this type of learning. We hypothesize that spontaneous activity in visual cortex gates incoming sensory information.

Opposing Somatic and Dendritic Expression of Stimulus-Selective Response Plasticity in Mouse Primary Visual Cortex

“…The only difference observed was a slight increase in active neurons during gray screen epochs that followed the presentation of the familiar visual stimulus, using the activity criteria of ≥10 events ( Table 3). This may reflect an increase in spontaneous neural activity following visual habituation, as previously reported (Miller et al, 2018).…”

A Platform for Brain-wide Volumetric Functional Ultrasound Imaging and Analysis of Circuit Dynamics in Awake Mice

“…Visualizing the whole brain requires stepping the probe across ll NeuroResource multiple positions, as recently demonstrated for identifying brain regions involved in the optokinetic reflex in awake mice (Mace ét al., 2018). However, this strategy involves long acquisition time and repetitive presentation of the stimulus at each position, which may hinder animal physiology and trigger habituation (Miller et al, 2018).…”

A Platform for Brain-Wide Functional Ultrasound Imaging and Analysis of Circuit Dynamics in Behaving Mice

“…Hence, we proved the high sensitivity of the vfUSI platform and showed that whisker-evoked hemodynamic responses are detectable in the cortex and the thalamic relay after an experimental session of 30 minutes maximum. Reducing the overall duration of an experiment and the number of stimuli is crucial to preserve proper animal physiology, animal comfort, and avoid the effects of habituation (Miller et al, 2018). Even if vfUSI has a voxel size ~2.5 times lower (~250 µm) compared to 2D fUSI (Figure S4), we were able to detect hemodynamic signals resulting from neuronal activation of functional units such as small individual cortical columns (~100 µm) during stimulation of a single whisker, or microcircuits processing orientation and directional selectivity during visual stimulation.…”

“…Visualizing the whole brain requires stepping the probe across multiple positions, as it was recently shown to identify brain regions involved in the optokinetic reflex in awake mice (Macé et al, 2018). This strategy, however, results in long acquisition time and repetitive presentation of the stimulus at each position, which may hinder animal physiology and trigger habituation (Miller et al, 2018).…”