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In the study of decision making, emphasis is placed on different forms of perceptual integration, while the influence of other factors, such as memory, is ignored. In addition, it is believed that the information underlying decision making is carried in the rate of the neuronal response, while its variability is considered unspecific. Here we studied the influence of recent experience on motor decision making by analyzing the activity of neurons in the dorsal premotor area of two monkeys performing a countermanding arm task. We observe that the across-trial variability of the neural response strongly correlates with trial history-dependent changes in reaction time. Using a theoretical model of decision making, we show that a trial history-monitoring signal can explain the observed behavioral and neural modulation. Our study reveals that, in the neural processes that culminate in motor plan maturation, the evidence provided by perception and memory is reflected in mean rate and variance respectively.

Neural activity was recorded in area PE (dorsorostral part of Brodmann's area 5) of the posterior parietal cortex while monkeys performed arm reaching toward memorized targets located at different distances from the body. For any given distance, arm movements were performed while the animal kept binocular eye fixation constant. Under these conditions, the activity of a large proportion (36%) of neurons was modulated by reach distance during the memory period. By varying binocular eye position (vergence angle) and initial hand position, we found that the reaching-related activity of most neurons (61%) was influenced by changing the starting position of the hand, whereas that of a smaller, although substantial, population (13%) was influenced by changes of binocular eye position (i.e., by the angle of vergence). Furthermore, the modulation of the neural activity was better explained expressing the reach movement end-point, corresponding to the memorized target location, in terms of distance from the initial hand position, rather than from the body. These results suggest that the activity of neurons in area PE combines information about eye and hand position to encode target distance for reaching in depth predominantly in hand coordinates. This encoding mechanism is consistent with the position of PE in the functional gradient that characterizes the parieto-frontal network underlying reaching.

Executive control of motor responses is a psychological construct of the executive system. Several studies have demonstrated the involvement of the cerebral cortex, basal ganglia, and thalamus in the inhibition of actions and monitoring of performance. The involvement of the cerebellum in cognitive function and its functional interaction with basal ganglia have recently been reported. Based on these findings, we examined the hypothesis of cerebellar involvement in executive control by administering a countermanding task in patients with focal cerebellar damage. The countermanding task requires one to make a movement in response to a ‘go’ signal and to halt it when a ‘stop’ signal is presented. The duration of the go process (reaction time; RT), the duration of the stop process (stop signal reaction time; SSRT), and their relationship, expressed by a psychometric function, are recorded as measures of executive control. All patients had longer go process duration in general and in particular, as a proactive control, as demonstrated by the increase in RT after erroneously performed stop trials. Further, they were defective in the slope of the psychometric function indicating a difficulty on triggering the stop process, although the SSRT did not differ from controls. Notably, their performance was worse when lesions affected deep cerebellar nuclei. Our results support the hypothesis that the cerebellum regulates the executive control of voluntary actions. We speculate that its activity is attributed to specific cerebellar influence over the cortico-striatal loop.

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