Hold your pauses: external globus pallidus neurons respond to behavioural events by decreasing pause activity

Abstract

Awareness of its rich structural pathways has earned the external segment of the globus pallidus (GPe) recognition as a central figure within the basal ganglia circuitry. Interestingly, GPe neurons are uniquely identified by the presence of prominent pauses interspersed among a high-frequency discharge rate of 50-80 spikes/s. These pauses have an average pause duration of 620 ms with a frequency of 13/min, yielding an average pause activity (probability of a GPe neuron being in a pause) of (620 × 13)/(60 × 1000) = 0.13. Spontaneous pause activity has been found to be inversely related to arousal state. The relationship of pause activity with behavioural events remains to be elucidated. In the present study, we analysed the electrophysiological activity of 200 well-isolated GPe pauser cells recorded from four non-human primates (Macaque fascicularis) while they were engaged in similar classical conditioning tasks. The isolation quality of the recorded activity and the pauses were determined with objective automatic methods. The results showed that the pause probability decreased by 9.09 and 10.0%, and the discharge rate increased by 2.96 and 1.95%, around cue and outcome presentation, respectively. Analysis of the linear relationship between the changes in pause activity and discharge rate showed r(2) = 0.46 and r(2) = 0.66 upon cue onset and outcome presentation, respectively. Thus, pause activity is a pertinent element in short-term encoding of relevant behavioural events, and has a significant, but not exclusive, role in the modulation of GPe discharge rate around these events.

Dynamic Encoding of Effort and Reward throughout the Execution of Action by External Globus Pallidus Neurons in Monkeys

“…The increase in neuronal activity at the population level after cues occur is consistent with previous findings (Deffains et al, 2016;Noblejas et al, 2015). Noblejas and colleagues have shown that the average GPe activity increases in response to relevant behavioral events.…”

Ethanol-Sensitive Pacemaker Neurons in the Mouse External Globus Pallidus

“…Interestingly, in humans, ethanol appears to decrease GPe activity, as evidenced by neuroimaging studies in which an oral dose of ethanol dampened the increase of GPe activity during a visual task and induced a slight decrease of GPe activity (Nikolaou et al , 2013). Although we are aware that GPe high-frequency neurons are characterized by interspersed pauses in monkeys (DeLong, 1971; Elias et al , 2007; Noblejas et al , 2015; Schechtman et al , 2015), we observed only occasional pausing behavior in some GPe neurons (data not shown). One reason for this difference may be species, as in rodents it has been reported that a subset of high-frequency neurons showed only occasional brief pauses (Dodson et al , 2015; Mallet et al , 2016).…”

Subthalamic nucleus stabilizes movements by reducing neural spike variability in monkey basal ganglia: chemogenetic study

“…Many GPe neurons reportedly exhibit pauses in non-human primates 33,40 and humans 41 . Although pauses were not correlated with any movements, relationships with alertness, task engagement, and motor learning have been reported [42][43][44] . Hence, the probability of pauses depends upon the animal's state, while the timing of individual pauses does not have any physiologic significance.…”