The striatum is the primary input nucleus of the basal ganglia, and alterations in striatal circuit function can produce a wide range of neurological and psychiatric disorders. Striatal projection neurons are under tight GABAergic regulation, of which the dominant component is thought to be provided by fast-spiking interneurons (FSIs). Blockade of striatal GABA transmission releases abnormal behaviors including dyskinesias and tic-like jerks, and a deficit in striatal FSIs has been observed in humans with tic disorders (Tourette syndrome) and rodents with dystonia. However, until recently little was known about the activity of FSIs in awake, behaving animals, or how these cells contribute to the behavioral functions of the basal ganglia. Investigations in my laboratory have revealed novel properties of FSIs that should help inform and constrain new computational models of both normal basal ganglia physiology and pathological conditions. Unlike projection neurons, FSIs show uniform changes in firing rate following administration of dopaminergic drugs that alter psychomotor activity, with the depressed activity of FSIs following D2 antagonists potentially contributing to the acute motoric side effects of antipsychotic medication. FSIs are coupled by gap junctions, leading to earlier suggestions that they may serve as a global feed-forward signal modulating striatal circuitry. Despite this, during performance of specific tasks even neighbouring FSIs show highly idiosyncratic firing rate time courses, consistent with participation in complex facets of local striatal information processing. We have found one moment at which FSIs seem to be co-modulated throughout striatum – when subjects begin to execute a choice between two highly trained actions. A pulse of enhanced FSI firing at this time coincides with a drop in globus pallidus (GP) activity, which is intriguing as there is a specific GABAergic projection from GP onto striatal FSIs. We suggest that the idiosyncratic aspect of FSI firing reflects unique focal sets of inputs from cortex, while the joint modulation of FSI firing reflects the operation of a more globally-directed pallidostriatal pathway that may be involved in the timing of action execution. I will also present evidence for distinctly different contributions of FSIs to striatal versus cortical microcircuits. In particular, the strong, fast FSI to projection neuron inhibition seen in striatal slices appears not to be constantly present in awake behaving animals, possibly due to high levels of short-term synaptic depression at natural firing frequencies. Emerging data suggest that, in addition to gross firing rate, precise temporal patterns of FSI firing may be critical for the organization of striatal projection neurons into functional ensembles.