Tonically discharging putamen neurons exhibit set-dependent responses.

Abstract

Previous microelectrode recordings in the putamen of monkeys have revealed a class of tonically active neurons without apparent behavioral correlates. The present study shows that such neurons have responses to stimuli that trigger movement but that these responses disappear when motor responses to the stimuli are extinguished. The short latency of the responses (less than for other putamen neurons) suggests that they may play a role in linking conditioned stimuli and responses.The putamen is an input stage for a group of interconnected subcortical neuronal aggregates collectively referred to as the basal ganglia. It receives inputs from the cerebral cortex and thalamus, is reciprocally connected with the substantia nigra pars compacta, and projects to the globus pallidus, a basal ganglia output stage. Microelectrode recordings in monkeys have shown that relatively few putamen neurons have tonic spontaneous discharge in the absence of movement; the more numerous putamen neurons that are phasically related to voluntary movement do not exhibit tonic activity in the absence of movement and, conversely, the tonically active neurons do not appear to be related to movement (1).The present study confirms the finding that tonic putamen neurons are unrelated to body movements per se, but it reveals that under certain circumstances they may exhibit highly reliable responses to external events. It was found that an auditory stimulus can elicit short-latency responses in tonic putamen neurons when the stimulus is a cue for juice delivery and consumption, but that such a stimulus fails to elicit responses when juice delivery has repeatedly failed to follow the sound, with the result that the sound no longer triggers movements associated with consuming the juice. MATERIALS AND METHODSTwo monkeys (Macaca mulatta) made repeated self-paced extension-flexion movements of the elbow for a juice reward that was delivered after eight movement cycles. The delivery of the reward was preceded by the click of a solenoid valve, which came to be a trigger for movements to consume the juice. Extracellular microelectrode recordings in the putamen yielded a number of tonic neurons that were unrelated to body movements and that had action potentials of greater duration (mean ± SD, 1.2 ± 0.2 msec) than action potentials of the more numerous putamen cells (0.9 ± 0.1 msec) that were silent except during movement. On casual inspection, these tonic neurons did not appear to be related to any aspect of the behavioral situation, but in raster displays aligned on the occurrence of the solenoid click that signaled reward (Fig. 1A), it was apparent that there was a greatly increased probability of impulse occurrence '60 msec after the click. This observation led to an examination of tonic neuron responsiveness in three behavioral conditions: (i) self-paced movement, as already described, in which a series of elbow movements resulted in a solenoid click and a juice reward; (ii) free reward, in which click and juice occurred at regular intervals (...

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). In addition, there is a greater recruitment of TANs during learning and possibly an enhanced coordination of these neurons (Aosaki, Tsubokawa, Ishida, Watanabe, Graybiel & Kimura, 1994).…”

“…The dynamic changes in the activity of TANs recorded from non-human primates have been commonly reported during initial acquisition of different associative learning tests (Kimura et al, 1984;Aosaki et al, 1994). In the rat dorsomedial striatum, changes in ACh efflux or muscarinic receptor effects have not been observed in the acquisition of discrimination tests, but during tests that require a shift in choice patterns.…”

Tonically Active Neurons in the Primate Caudate Nucleus and Putamen Differentially Encode Instructed Motivational Outcomes of Action

“…The action potentials of single neurons were isolated by using a spike sorter with a template-matching algorithm (multi-spike detector; Alpha Omega Technologies, Nazareth, Israel), and the onset times of the action potentials were recorded on a laboratory computer (9801BX4; NEC, Tokyo, Japan) together with the onset and offset times of stimuli and the behavioral events that occurred in association with the tasks. We identified TANs on the basis of their tonic firing (2-8 Hz) and their broad action potentials (Kimura et al, 1984;Apicella et al, 1991;Aosaki et al, 1994). Electromyographic (EMG) activity was recorded from the extensor, flexor, and biceps brachii muscles of the right arm as well as from the digastric muscle through chronically implanted multithreaded Teflon-coated stainless-steel wire electrodes (AS631; Cooner Wire, Chatsworth, CA) with leads that led subcutaneously to the head implant.…”

“…Projection neurons code expectation of rewards (Hikosaka et al, 1989;Schultz et al, 1992;Tremblay et al, 1998;Lauwereyns et al, 2002), kinds of rewards (Hassani et al, 2001), magnitude of rewards (Cromwell and Schultz, 2003), and proximity of rewards (Shidara et al, 1998;Jog et al, 1999). Tonically active neurons (TANs), presumed cholinergic interneurons in the striatum (Wilson et al, 1990;Aosaki et al, 1995;Kawaguchi et al, 1995), were initially characterized by the responses to reward-associated stimuli (Kimura et al, 1984;Apicella et al, 1991;Kimura, 1992;Raz et al, 1996), by the evolution of responses via behavioral learning (Aosaki et al, 1994b), and by the involvement of the nigrostriatal dopaminergic system in the responses (Aosaki et al, 1994a). It was subsequently shown that TANs respond not only to reward-associated stimuli but also to aversive stimuli such as an airpuff on the face (Ravel et al, 1999;Blazquez et al, 2002;Ravel et al, 2003).…”

Response of caudate neurons to stimulation of intrinsic and peripheral afferents in normal, symptomatic, and recovered MPTP-treated cats

“…We (Schneider and Lidsky, 198 1;Lidsky et al, 1985;Schneider, 1987) and others (Kimura et al, 1984;Apicella et al, 1991;Ljungberg et al, 1991;Schwarz et al, 1992) have suggested that sensory processing is an important aspect of basal ganglia function and hence normal basal ganglia modulation of motor behavior. We would then expect that sensory responsiveness of striatal neurons would recover coincident with recovery of gross motor function.…”