Functional consequences of fast-spiking interneurons in striatum

Abstract

The striatum features a distinct network characterized by a high degree of shared feedforward inhibition (FFI) from a mere 1% of fast-spiking interneurons (FSI). We investigate the potential roles of this extensively shared FFI in striatal function beyond inducing synchrony. Our findings reveal that FSIs increase the acrosstrial variability of striatal responses to cortical stimuli and, combined with recurrent inhibition, lead to a correlation attractor of striatal activities, i.e., weakly correlated inputs result in more correlated responses and vice versa. Thus, we uncover a mechanism by which input correlation can be bidirectionally modulated, which is possible only because of high sharing of FSI inputs. We posit that the emergence of a correlation attractor leads to non-zero correlation level and variable rate trajectories of striatal responses across trials, hence beneficial for exploration in learning. However, given their role in across-trial variability, we argue that FSIs should be disengaged from the MSNs during performance where stability across trials is required. Significance StatementStriatum is a network of inhibitory neurons. Fast spiking interneurons constitute about 1% of the striatal neural population and provide feedforward inhibition (FSI). Here, we unravel two novel ways in which FSIs may shape striatal function. Given the recurrent inhibition, it is assumed that striatum can only de-correlate inputs. We show that high sharing of FSI also renders the striatum an ability to correlate inputs. Thus, recurrent and shared FSI create a correlation attractor. Besides, we show that shared FSIs give rise to high across-trial variability. Therefore, we argue that FSIs are more crucial in learning as they provide the neural basis of exploration, but they may impair learned behavior due to high across-trial variability.