Membrane properties and synaptic connectivity of fast-spiking interneurons in rat ventral striatum

Abstract

In vitro patch-clamp recordings were made to study the membrane properties and synaptic connectivity of fast-spiking interneurons in rat ventral striatum. Using a whole-cell configuration in acutely prepared slices, fast-spiking interneurons were recognized based on their firing properties and their morphological phenotype was confirmed by immunocytochemistry. Membrane properties of fast-spiking interneurons were distinguished from those of medium-sized spiny neurons by their more depolarized resting membrane potential, lower action potential amplitude and shorter half-width, short spike repolarization time and deep spike afterhyperpolarization. Firing patterns of interneurons could be subdivided in a bursting and non-bursting mode. Simultaneous dual whole-cell recordings revealed a high degree of connectivity of fast-spiking interneurons to medium-sized spiny neurons via unidirectional synapses. Burst firing in fast-spiking interneurons that were presynaptic to medium-sized spiny neurons resulted in barrages of postsynaptic potentials showing an initial amplitude increment, rapidly followed by a decrement. In conclusion, ventral striatal fast-spiking interneurons can be clearly distinguished from medium-sized spiny neurons by their membrane properties and their firing patterns can be subdivided in bursting and non-bursting modes. Their synaptic connectivity to medium-sized spiny neurons is unidirectional and characterized by frequency-dependent, dynamic changes in postsynaptic amplitude.

Introduction

Fast-spiking interneurons (FSIs) constitute a class of interneurons of the ventral striatum (VS), a component of the striatum that plays a role in expressing and adjusting goal-directed and emotional behaviour (Mogenson et al., 1980, Pennartz et al., 1994, Cardinal et al., 2002, Carelli, 2002, Nicola et al., 2004a, Nicola et al., 2004b). FSIs contain aspiny dendrites, emit axon collaterals that spread locally but may also reach relatively distant subregions of the striatum, and express the calcium-buffering protein parvalbumin (PV; Kawaguchi, 1993, Kawaguchi et al., 1995). Striatal FSIs are thought to exert inhibitory control over the excitability of the principal cells of the striatum, i.e. medium-sized spiny neurons (MSNs; Kita et al., 1990, Pennartz and Kitai, 1991, Kita, 1996, Plenz and Kitai, 1998, Koos and Tepper, 1999, Koos et al., 2004). Patch-clamp studies in the dorsal striatum have shown that FSIs are characterized by ‘fast’ (i.e. short-lasting) action potentials discharged at high maximal rates (∼ 200 Hz), prominent frequency accommodation when moderately depolarized, a relatively large spike afterhyperpolarization (AHP) and subthreshold oscillations occurring at a frequency of ∼ 40 Hz (Kawaguchi, 1993, Koos and Tepper, 1999). Dual-cell recordings in cultured (Plenz and Kitai, 1998) and acutely prepared striatal slices (Koos and Tepper, 1999, Koos and Tepper, 2002, Koos et al., 2004) presented evidence for GABA_A receptor mediated inhibition by FSIs onto MSNs. In vitro, this inhibition is expressed by way of blocking or delaying postsynaptic firing of action potentials (Koos and Tepper, 1999). An additional type of interaction, which has been indicated by recordings in hippocampus but has not been documented for the striatum, is that an initial inhibition of principal cells by FSIs is followed by a rebound excitation (Buhl et al., 1995, Cobb et al., 1995). In view of anatomical and electrophysiological evidence, it has been suggested that FSIs in the VS provide feed-forward inhibition of MSNs, primarily by rapid shunting of glutamatergic limbic and prefrontal inputs and thus imposing a temporal window for suppressing postsynaptic excitability and synaptic plasticity in MSNs (Pennartz and Kitai, 1991, Pennartz et al., 1993, Pennartz et al., 1994). It remains unknown, however, whether the membrane properties and connectivity of FSIs in the VS are similar to those in the dorsal striatum. A separate investigation of FSIs in the VS is warranted considering recently presented functional differences in entrainment of FSI firing to EEG rhythms in the dorsal and ventral striatum in vivo (Berke et al., 2004). The present paper describes the basic membrane properties of FSIs in the VS and their synaptic connections to medium-sized spiny neurons. In particular, the current findings highlight the bursting capacity of at least a subgroup of FSIs as well as a dynamic, frequency-dependent effect in the amplitude of synaptic potentials observed in MSNs following presynaptic burst firing of FSIs.