Relationship between EEG Potentials and Intracellular Activity of Striatal and Cortico-striatal Neurons: an In Vivo Study under Different Anesthetics

Abstract

The functions of the basal ganglia are achieved through excitation of striatal output neurons (SONs) by converging cortical glutamergic afferents. We assessed the relationship between different patterns of activity in cortico-striatal (C-S) cells and the electrical behavior of SONs in vivo. Intracellular activities of rat C-S neurons in the orofacial motor cortex and of SONs, located in the projection field of this cortical region, were recorded under different anesthetics, which generate various temporal patterns of cortical activity. A surface electroencephalogram (EEG) of the orofacial motor cortex was simultaneously performed with intracellular recordings and EEG waves were used as correlates of a coherent synaptic activity in cortical neurons. Under barbiturate anesthesia C-S neurons showed rhythmic (5--7 Hz) supra-threshold depolarizations in phase with large amplitude EEG waves. The correlative activity of SONs was characterized by large amplitude oscillation-like synaptic depolarizations that could trigger action potentials. Under ketamine-xylazine anesthesia C-S neurons exhibited a step-like behavior consisting of depolarizing plateaus (up states), leading to multiple spike discharges, interrupted by hyperpolarizing periods (down states). The related activity of SONs was step-like membrane potential fluctuations with firing confined to the early part of the striatal up state. In C-S neurons and SONs up states coincided with slow recurrent EEG waves (approximately 1 Hz). Finally, under neurolept-analgesia an apparently disorganized EEG activity was associated with a lack of rhythmic discharge in C-S neurons. This uncorrelated activity in C-S neurons resulted in an absence of spontaneous firing as well as of large amplitude synaptic depolarizations in SONs. In the present study we demonstrate that SONs shape their input-output relationship by filtering out uncorrelated synaptic activity and that a minimal synchronization in the cortico-striatal afferents is required to produce significant synaptic depolarization in SONs.

Phase relationships support a role for coordinated activity in the indirect pathway in organizing slow oscillations in basal ganglia output after loss of dopamine

“…The firing patterns observed in the striatum in these recordings are consistent with a considerable body of literature which has shown that striatal activity in anesthetized preparations is organized into 'up-states' and 'down-states' by slow, ∼1 Hz oscillations in cortical activity (Wilson and Kawaguchi, 1996;Stern et al, 1997;Mahon et al, 2001;Tseng et al, 2001b;Murer et al, 2002;Goldberg et al, 2003). The increase in spikes per burst in striatal spike trains in the present study in lesioned rats is consistent with an intracellular recording study by Tseng, Murer and colleagues (Tseng et al, 2001b;Murer et al, 2002), which found that a population of striatal neurons is more depolarized after dopamine cell lesion and has an increased probability of firing in the 'up-state', leading to an increased number of spikes per oscillatory cycle.…”

On the Activity of the Corticostriatal Networks during Spike-and-Wave Discharges in a Genetic Model of Absence Epilepsy

“…Membrane potential of SONs, measured between SWDs, was Ϫ76.8 Ϯ 1.4 mV (n ϭ 10 cells). These membrane properties are similar to those described previously in vivo from nonepileptic rats (Wilson, 1995;Charpier et al, 1999;Mahon et al, 2001Mahon et al, , 2003. This finding suggests that changed neuronal membrane properties did not underlie the inability of GAERS striatal output neurons to fire action potentials during SWDs.…”

“…1 A, inset) was characteristic of "regularspiking" neocortical neurons (Connors and Gutnick, 1990). These electrophysiological properties of CS neurons agree with those measured previously in crossed CS neurons from nonepileptic rats (Cowan and Wilson, 1994;Mahon et al, 2001).…”

“…Spontaneous events were composed of highfrequency, small-amplitude, depolarizing synaptic potentials (Figs. 4 A, 5A, 6A) resembling those recorded in vivo in normal rats under fentanyl (Mahon et al, 2001). This intracellular activity of SONs noticeably differs from the two-state behavior observed under ketamine-xylazine anesthesia, i.e., characteristic shifts of membrane potential between a hyperpolarized downstate and depolarized upstate (Wilson, 1995;Wilson and Kawaguchi, 1996;Stern et al, 1997;Mahon et al, 2001), which are associated with rhythmic largeamplitude EEG waves (Mahon et al, 2001).…”

“…Because action potential firing in SONs is naturally and consistently initiated by excitatory synaptic potentials generated by synchronized corticostriatal inputs (Wilson, 1995;Wilson and Kawaguchi, 1996;Stern et al, 1997;Mahon et al, 2001), this absence of firing during SWDs was unexpected. Therefore, we performed intracellular records (n ϭ 10) to explore cellular and synaptic mechanisms controlling SON activity during absence seizures.…”