Mechanisms of Action Selection and Timing in Substantia Nigra Neurons

Abstract

The timing of actions is critical for adaptive behavior. In this study we measured neural activity in the substantia nigra as mice learned to change their action duration to earn food rewards. We observed dramatic changes in single unit activity during learning: both dopaminergic and GABAergic neurons changed their activity in relation to behavior to reflect the learned instrumental contingency and the action duration. We found the emergence of "action-on" neurons that increased firing for the duration of the lever press and mirrorimage "action-off" neurons that paused at the same time. This pattern is especially common among GABAergic neurons. The activity of many neurons also reflected confidence about the just completed action and the prospect of reward. Being correlated with the relative duration of the completed action, their activity could predict the likelihood of reward collection. Compared with the GABAergic neurons, the activity of dopaminergic neurons was more commonly modulated by the discriminative stimulus signaling the start of each trial, suggesting that their phasic activity reflected sensory salience rather than any reward prediction error found in previous work. In short, these results suggest that (1) nigral activity is highly plastic and modified by the learning of the instrumental contingency; (2) GABAergic output from the substantia nigra can simultaneously inhibit and disinhibit downstream structures, while the dopaminergic output also provide bidirectional modulation of the corticostriatal circuits; (3) dopaminergic and GABAergic neurons show similar task-related activity, although DA neurons are more responsive to the trial start signal.

Action, time and the basal ganglia

“…B 369: 20120473 pressing ( figure 3a). In other words, the reward delivery is contingent upon press duration, rather than press rate, as in traditional operant conditioning [32,35,36]. Press duration can be used to tag the neural activity generating the action itself [33,35].…”

“…Using temporal differentiation, we studied the neural activity of GABAergic output neurons in the SNr and of the nearby dopaminergic neurons in the pars compacta [35]. We found two major neural activity patterns in relation to the lever press action in the recorded neurons: in one type of neurons ('action-on') there was a sustained increase in firing rate during the action, and in the other population ('action-off') there was a sustained pause in firing rate during the press (figure 3).…”

“…Muscle tension is sensed by the Golgi tendon organs, which send Ib afferents representing the negative feedback for the force control system. In this connection, it is worth noting that increased stiffness in skeletal muscles is also observed in Parkinson's patients, as a result [33,35]. Mice must press a lever and hold it down for a minimum amount of time in order to earn a food pellet.…”

Prefrontal cortical mechanisms underlying delayed alternation in mice

“…Prefrontal cortical mechanisms underlying delayed alternation in mice. J Neurophysiol 108: 1211-1222, 2012. First published April 25, 2012 doi:10.1152/jn.01060.2011The prefrontal cortex (PFC) has been implicated in the maintenance of task-relevant information during goal-directed behavior.…”

“…Using operant conditioning methods (Fan et al 2012;Yin 2009;Yu et al 2009), we trained mice to press one lever and a different lever after a predetermined delay for food rewards. This task introduces a delay between two actions in a behavioral sequence and a simple "switching" rule (AB or BA), so that the mouse must remember which action it just completed to choose the next action correctly (Mizumori et al 1987).…”