Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum

Abstract

Interneurons in lateral part of neostriatum were studied in isolated slices from juvenile rats (16–20 d postnatal) by whole-cell, current- clamp recording at 33–34 degrees C, followed by intracellular staining with biocytin and double immunocytochemical or histochemical staining for parvalbumin, ChAT, and NADPH diaphorase. Medium-sized spiny neurons (MS cells) had distal dendrites with many spines and were likely projection cells, while interneurons had dendrites with fewer spines. The neostriatal interneurons could be further divided into three classes by physiological, chemical, and morphological criteria. The first class of interneurons (fast-spiking cells, FS cells) fired very short-duration action potentials with short-duration afterhyperpolarizations at constant spike frequency during depolarizing current pulses. FS cells had more negative resting potentials and lower input resistances than the other two classes. At depolarized potentials, FS cells fired repetitive spikes in response to synaptic excitation. FS cells were immunoreactive for parvalbumin. As all parvalbumin-immunoreactive cells in the neostriatum were also immunoreactive for GABA, FS cells were considered to be GABAergic. FS cells were further divided into two morphological types: FS cells with local dendritic fields and FS cells with extended dendritic fields. The axons of both types of FS cells had their densest collateralization within or near their dendritic fields. The other two classes of interneuron, PLTS cells (persistent and low-threshold spike cells) and LA cells (long-lasting afterhyperpolarization cells), were distinguished from FS cells by longer-duration action potentials and larger input resistances, had less negative resting potentials, and had longer-lasting afterhyperpolarizations. Afterhyperpolarizations of PLTS cells had a shorter time to peak than those of LA cells. PLTS cells fired both Na(+)-dependent, persistent depolarization spikes and Ca(2+)- dependent, low-threshold spikes in addition to fast spikes. Low- threshold spikes in PLTS cells were induced only from hyperpolarized potentials. Both persistent depolarizations and low-threshold spikes could also be evoked by synaptic activation. PLTS cells were histochemically identified as NADPH diaphorase-positive cells. As all NADPH diaphorase-positive cells in the same tissue were immunoreactive for nitric oxide (NO) synthase, PLTS cells were considered to release NO. PLTS cells had the largest axonal fields. Some PLTS cells appeared to have two axonal origins from the somata and dendrites. LA cells were mostly large aspiny cells with Ca(2+)-dependent long-lasting afterhyperpolarizations and strong time-dependent hyperpolarizing rectification. As this slowly occurring anomalous rectification was blocked by 2 mM cesium, this potential was considered to be due to activation of Ih.(ABSTRACT TRUNCATED AT 400 WORDS)