Temporal and spatial characteristics of tonically active neurons of the primate's striatum

Abstract

1. Tonically active neurons (TANs) in the primate striatum develop transient responses to sensory conditioning stimuli during behavioral training in classical conditioning tasks. In this study we examined the temporal characteristics of such TAN responses and mapped the sites of TANs responding to auditory and visual conditioned stimuli in the striatum in macaque monkeys. We further mapped the locations of TANs recorded acutely in the squirrel monkey striatum in relation to the neurochemically distinguished striosome and matrix compartments of the striatum, and made quantitative comparisons between the densities and compartmental distributions of TANs and those of four major types of striatal interneuron identified by histochemical and immunohistochemical staining. 2. We made recordings from 858 TANs at different sites in the striatum in two behaving macaque monkeys at different times during training with auditory (click) and visual (light-emitting diode flash) conditioning stimuli. TANs distributed across large parts of the striatum developed responses to the conditioning stimuli. The responses comprised a decrement of tonic firing (pause) followed by a rebound excitation. Measurements were made of the onsets, offsets, and durations of the pauses of individual TANs and of the interspike intervals (ISIs) of the same cells. 3. The mean duration of the pause responses (268.3 ms) was greater than the mean ISI of the same neurons (181 ms), suggesting that the pause represents an active suppression of TAN firing. The coefficient of variation (CV) for the pause responses was 0.28, compared with a CV of 0.63 for the same cells' ISIs. The population CV for the pauses was 0.16, compared with a population CV of 0.20 for the ISIs. These data, together with temporal analysis of the responses and population histograms, suggest that the pauses became temporally aligned across large parts of the striatum after learning. Analyses of variance (ANOVAs) were carried out to determine whether there were differences in the onset and offset latencies of the pause response or in the durations of the pause responses for TANs at different sites. These analyses suggested that, with rare exceptions, there was no difference in the timing of the TAN responses across large (> 10 mm3) parts of the striatum. 4. Comparisons of TAN responses in different regions of the striatum showed that, for responses to a given modality of conditioned stimulus, there were no significant differences in pause offset times for TANs recorded in the caudate nucleus or putamen, or for TANs recorded in more anterior or more posterior parts of these nuclei.(ABSTRACT TRUNCATED AT 400 WORDS)

Differential involvement of M1-type and M4-type muscarinic cholinergic receptors in the dorsomedial striatum in task switching

“…At a neurophysiological level, the cholinergic interneurons are thought to be the tonically active neurons (TANs) [Aosaki et al, 1994[Aosaki et al, , 1995Graybiel, 1995Graybiel, , 1998Wilson, Chang & Kitai, 1990]. These neurons commonly exhibit an initial and transient decrease in activity following a conditioned stimulus and subsequently a rebound in activation (Kimura et al, 1984;Ravel, Legallet & Apicella, 1999;Ravel, Sardo, Legallet & Apicella, 2001).…”

Cholinergic interneuron characteristics and nicotinic properties in the striatum

“…The irregular single spiking pattern matched the pattern of activity observed in vivo with anesthestized rats, and in the majority of descriptions of tonically active neurons in behaving animals. The rhythmic single spiking pattern and the rhythmic bursting patterns have also been reported in behaving animals (Aosaki et al, 1995;Raz et al, 1996). The ionic mechanisms underlying the rhythmic single spiking pattern have been mostly characterized, and depend mainly on depolarization by a subthreshold persistent sodium current and a long spike afterhyperpolarization generated by calcium-dependent potassium current (Bennett et al, 2000).…”

“…The dense AChE rapidly terminates the ACh signal so that the nAChRs are not strongly desensitized. By minimizing desensitization, the nAChRs are able to participate continually as the ACh pulses arrive at about 5 Hz (Aosaki et al, 1995;Bennett and Wilson, 1999). The small number of cholinergic interneurons with large axonal arbors enables one or a few interneurons to synchronize the DA release in a large volume of tissue.…”

“…Sometimes the pause in tonic activity is preceded by a brief increase in firing rate, but this is not consistently observed (Aosaki et al, 1995). After the pause, the firing rate often increases, resembling a rebound.…”

“…A key difference between the phasically active spiny neurons and tonically active cholinergic interneurons is that there is a different sign to the change in their firing rates during a conditioned movement. In addition, the firing rate change of cholinergic interneurons is not closely related to the execution of tasks, but rather to the presentation of the conditioned, trigger stimulus (Aosaki et al, 1995). However, the firing is not simply sensory in nature because the cholinergic interneurons acquire their responses during conditioning, and their responses undergo extinction along with the conditioned movement (Aosaki et al, 1994a(Aosaki et al, , 1994b.…”