Intrinsic properties of rat striatal output neurones and time-dependent facilitation of cortical inputs in vivo.

Abstract

Listen

Translate article

The striatum, the main input stage of the basal ganglia, integrates monosynaptic glutamatergic inputs originating from widespread areas of cerebral cortex (McGeorge & Faull, 1989; Deniau et al. 1996). Despite this powerful synaptic excitation, striatal output neurones (SONs), the major class of striatal neurones, exhibit a low rate of firing activity (Wilson, 1995; Charpier et al. 1999). It is assumed that this low excitability of SONs is due to a set of voltage-dependent potassium currents (Nisenbaum et al. 1994; Nisenbaum & Wilson, 1995; Wilson, 1995) acting as an inhibitory shunt on excitatory inputs rather than due to competing synaptic inhibition (Jaeger et al. 1994). A distinctive electrophysiological property of SONs is their delayed firing in response to intracellular injection of a threshold current pulse. This has been attributed to a calcium-independent potassium A current (IAs) available around −60 mV that inactivates and recovers from inactivation slowly (Nisenbaum et al. 1994; Gabel & Nisenbaum, 1998). Similar slowly inactivating outward potassium currents have also been described in other central neurones, including hippocampal CA1 pyramidal neurones (ID; Storm, 1988), thalamic lateral geniculate nucleus relay neurones (IAs; McCormick, 1991) and prefrontal cortical neurones (IKs; Hammond & Crepel, 1992). It is proposed that such currents limit the initial response to depolarising inputs and, by inactivating, slowly permit the membrane to depolarise towards the spike threshold. In addition, it has been hypothesised that the slow recovery from inactivation of these currents would produce a time-dependent facilitation in synaptic integration after strong depolarising inputs (Storm, 1988; Turrigiano et al. 1996). However, evidence that synaptic events in an intact brain could be reinforced through use-dependent modulation of such slow potassium currents is lacking. Therefore, the aim of the present in vivo study was to test whether the efficacy of cortico-striatal connections can be enhanced following strong depolarising inputs. Here, we show that a prior depolarisation of SONs induces a short-term increase in their intrinsic excitability, expressed as a facilitation of action potential firing in response to intracellular current pulses. This use-dependent increase in cell responsiveness can transform subthreshold cortically evoked excitatory postsynaptic potentials (EPSPs) into suprathreshold inputs and thus strongly influence the input-output relationship of the SONs. The putative role of IAs in the time-dependent increase in SON excitability is discussed.