Abstract
Habit formation is a behavioral adaptation that automates routine actions. Habitual behavior correlates with broad reconfigurations of dorsolateral striatal (DLS) circuit properties that increase gain and shift pathway timing. The mechanism(s) for these circuit adaptations are unknown and could be responsible for habitual behavior. Here we find that a single class of interneuron, fast-spiking interneurons (FSIs), modulates all of these habit-predictive properties. Consistent with a role in habits, FSIs are more excitable in habitual mice compared to goal-directed and acute chemogenetic inhibition of FSIs in DLS prevents the expression of habitual lever pressing. In vivo recordings further reveal a previously unappreciated selective modulation of SPNs based on their firing patterns; FSIs inhibit most SPNs but paradoxically promote the activity of a subset displaying high fractions of gamma-frequency spiking. These results establish a microcircuit mechanism for habits and provide a new example of how interneurons mediate experience-dependent behavior.
Highlights
Habit formation is an adaptive behavioral response to frequent and positively reinforcing experiences
To first approximate how fastspiking interneurons (FSIs) modulate the habit-predictive properties of evoked striatal output, the same ex vivo population calcium imaging approach that identified the behavior-predictive properties (O’Hare et al, 2016) was used on tissue prepared from untrained animals (Figure 1A,B)
The potential for FSIs themselves to exhibit long-lasting activity-dependent plasticity is well-documented in acute brain slice experiments (Mathur et al, 2013; Orduz et al, 2013; Hainmuller et al, 2014; Sarihi et al, 2012; Dehorter et al, 2015), we are aware of only one report in which these interneurons were found to undergo experience-dependent plasticity and contribute to the expression of an adaptive behavior or memory (Donato et al, 2013)
Summary
Habit formation is an adaptive behavioral response to frequent and positively reinforcing experiences. Habits allow routine actions to be triggered by external cues. This automation frees cognitive resources that would otherwise process action-outcome relationships underlying goal-directed behavior. Properties of the dorsolateral striatum (DLS) input-output transformation of afferent activity to striatal projection neuron firing were found to predict the extent of habitual behavior in individual animals (O’Hare et al, 2016). Despite these observations, the cellular microcircuit mechanisms driving habitual behavior have not been identified
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