Direct Physiological Evidence for Synaptic Connectivity Between Medium-Sized Spiny Neurons in Rat Nucleus Accumbens In Situ

Abstract

Dual whole cell patch-clamp recordings in rat nucleus accumbens, the main component of the ventral striatum, were made to assess the presence of synaptic interconnections between medium-sized spiny neurons, a group of GABAergic and peptidergic neurons that constitute the principal cells of the striatum. Neurons were stained with biocytin for subsequent morphological analysis. Electrical activity of cells was recorded in current- and voltage-clamp mode; the characteristics of medium-sized spiny neurons were confirmed by electrophysiological and morphological properties. Thirteen of 38 medium-sized spiny neuron pairs (34%) showed a synaptic connection. In these pairs, suprathreshold stimulation with current injection evoked a train of action potentials in the presynaptic cell, which in turn elicited depolarizing postsynaptic potentials (dPSPs) in the postsynaptic cell. Twelve of these 13 pairs were connected unilaterally. The onset latency of the postsynaptic response was 1.7 ± 0.7 ms. dPSPs were blocked by 12.5 μM bicuculline, suggesting they were mediated by GABAA receptors. A linear fit of the current-voltage relationship of GABAergic currents crossed the voltage axis near the value of -20 mV, in agreement with the Cl- equilibrium potential predicted from the composition of the artificial cerebrospinal fluid and pipette medium. No evidence for electrotonic coupling was found. Paired-pulse facilitation and depression were induced when the amplitude of the first IPSC of a pair was relatively small and large, respectively. No clear dependence of paired-pulse facilitation or depression was found on the width of the spike interval, which ranged between 100 and 380 ms. Conversely, 1- to 2-s trains of dPSPs showed marked frequency facilitation at low presynaptic frequencies, but frequency depression at high firing rates. These data show that intra-accumbens synaptic communication between medium-sized spiny neurons exists, is mediated by GABAA receptors, and exhibits spike train-dependent short-term dynamics.