Firing patterns and synaptic potentials of identified giant aspiny interneurons in the rat neostriatum

Abstract

Intracellular recordings were made in vivo from 9 giant aspiny neurons in the neostriatum of urethane-anesthetized rats. The cells were identified by intracellular staining with HRP or biocytin. The neurons exhibited morphological features typical of neostriatal cholinergic interneurons. Six of the cells were obtained from intact animals, while 3 were recorded from rats with ipsilateral hemidecortications. Giant aspiny neurons were characterized by their slow irregular but tonic (3–10/sec) spontaneous activity and long-duration action potentials. Examination of the underlying membrane potential trajectories during spontaneous firing revealed that individual action potentials were triggered from spontaneous small (1–5 mV) depolarizing potentials. These spontaneous potentials exhibited the voltage sensitivity of ordinary EPSPs. They were much less frequent during the 80–200 msec pause in tonic afferent input that follows the excitation evoked by cortical or thalamic stimulation, and were decreased in frequency in decorticate animals. Their rise times and half-widths matched those expected for unitary synaptic potentials placed proximally on the surface of the neurons. Low-intensity stimulation of neostriatal afferents produced small short-latency EPSPs that appeared to be composed of responses identical to the spontaneous depolarizing potentials. The latencies of the EPSPs evoked from the cerebral cortex and thalamus were consistent with a monosynaptic input from both structures, but the maximal size of the EPSPs was much smaller than that evoked in spiny neurons, suggesting that a smaller number of afferent inputs make synapses with each of the aspiny cells. Giant aspiny neurons exhibited much larger input resistances and longer time constants than spiny neostriatal neurons. They also exhibited relatively linear steady-state current-voltage relationship compared to spiny projection cells. Input resistances ranged from 71–105 M omega, and time constants ranged from 17.8–28.5 msec. Analysis of the charging transients in response to current pulses yielded estimates of dendritic length of approximately 1 length constant. Repetitive firing of the neurons was limited by a powerful spike afterhyperpolarization and by a strong spike frequency adaptation. The sensitivity of the giant aspiny interneuron to a relatively small number of proximal afferent synaptic contacts, its tonic firing, and its widespread dendritic and axonal fields place it in an excellent position to act as a modulator of the excitability of neostriatal projection neurons in advance of the onset of movement-related neostriatal activity.