Functional properties of striatal fast-spiking interneurons

Abstract

Striatal fast-spiking interneurons (FSIs) have a major influence over behavioral output, and a deficit in these cells has been observed in dystonia and Tourette syndrome. FSIs receive cortical input, are coupled together by gap junctions, and make perisomatic GABAergic synapses onto many nearby projection neurons. Despite being critical components of striatal microcircuits, until recently little was known about FSI activity in behaving animals. Striatal FSIs are near-continuously active in awake rodents, but even neighboring FSIs show uncorrelated activity most of the time. A coordinated "pulse" of increased FSI firing occurs throughout striatum when rats initiate one chosen action while suppressing a highly trained alternative. This pulse coincides with a drop in globus pallidus population activity, suggesting that pallidostriatal disinhibition may have a important role in timing or coordinating action execution. In addition to changes in firing rate, FSIs show behavior-linked modulation of spike timing. The variability of inter-spike intervals decreases markedly following instruction cues, and FSIs also participate in fast striatal oscillations that are linked to rewarding events and dopaminergic drugs. These studies have revealed novel and unexpected properties of FSIs, that should help inform new models of striatal information processing in both normal and aberrant conditions.

Keywords: GABA; amphetamine; antipsychotic; basal ganglia; dopamine; gamma oscillations; interneuron; striatum.

Figure 1

Stabilization of FSI firing pattern with action programming. This example shows activity of a single striatal FSI during performance of an instructed left/right choice task (Gage et al., 2010). Upper panels show raster plots (151 trials total), lower panels show peri-event histograms of firing rate (time range: –0.5 to 0.5s in each case). The rat begins the trial by inserting his nose into an illuminated port (Nose In) and waits for an instruction cue (Tone) that indicates whether a subsequent left or right movement will be rewarded, provided the rat waits for a second cue (Go) before initiating his movement (Choice). For the raster aligned on the Go cue, trials are ordered by reaction time. The FSI shows a sharp increase in firing rate beginning shortly before movement onset, that in this case is stronger for ipsilateral (green) than contralateral movements (gold). The onset of the tone is not associated with a substantial firing rate change, but causes the cell to spike far more regularly until the action is executed (for quantitative analysis, see Lau et al., 2010).