Roles of Monkey Premotor Neuron Classes in Movement Preparation and Execution

Abstract

Dorsal premotor cortex (PMd) is known to be involved in the planning and execution of reaching movements. However, it is not understood how PMd plan activity-often present in the very same neurons that respond during movement-is prevented from itself producing movement. We investigated whether inhibitory interneurons might "gate" output from PMd, by maintaining high levels of inhibition during planning and reducing inhibition during execution. Recently developed methods permit distinguishing interneurons from pyramidal neurons using extracellular recordings. We extend these methods here for use with chronically implanted multi-electrode arrays. We then applied these methods to single-and multi-electrode recordings in PMd of two monkeys performing delayed-reach tasks. Responses of putative interneurons were not generally in agreement with the hypothesis that they act to gate output from the area: in particular it was not the case that interneurons tended to reduce their firing rates around the time of movement. In fact, interneurons increased their rates more than putative pyramidal neurons during both the planning and movement epochs. The two classes of neurons also differed in a number of other ways, including greater modulation across conditions for interneurons, and interneurons more frequently exhibiting increases in firing rate during movement planning and execution. These findings provide novel information about the greater responsiveness of putative PMd interneurons in motor planning and execution and suggest that we may need to consider new possibilities for how planning activity is structured such that it does not itself produce movement.

Enhanced sensory sampling precedes self-initiated locomotion in an electric fish

“…Cortical recordings reveal that neural activity precedes the time when a conscious decision to act is reported (Kornhuber and Deecke, 1965;Libet et al, 1983;Soon et al, 2008), raising questions as to how neural activity relates to conscious decision making and the initiation of voluntary actions. Whereas prior work has shown neural activity preceding voluntary actions in primates capable of advanced cognition (Romo and Schultz, 1987;Kato et al, 1995;Kaufman et al, 2010), here we demonstrate the same pattern in an aquatic vertebrate whose last common ancestor to primates lived more than 450 million years ago. We propose that volition may therefore be a primitive capability of vertebrate brains that precedes the advanced cognitive capacities of primates.…”

“…Sustained preparatory neural activities preceding voluntary movements have been reported in humans (Kornhuber and Deecke, 1965;Libet et al, 1983;Soon et al, 2008) and monkeys (Romo and Schultz, 1987;Kato et al, 1995;Kaufman et al, 2010). Here, however, we further demonstrate that the increased neural activity preceding self-initiated movement is also associated with a heightened sensory sampling (EODR) that precedes movement onset.…”

“…Preparatory neural activities for voluntary movements involve movement planning and decision making (Kaufman et al, 2010), and voluntary control of active sensory sampling accompanies heightened spatial attention (Winkowski and Knudsen, 2006;Ulanovsky and Moss, 2008). Here, we show that enhanced sensory sampling precedes the voluntary decision to move in an animal model that exhibits a readily observable and quantifiable sensory acquisition rate.…”

“…Through behavioural down-to-up transitions, such movements are also correlated with the increased variability of neural activity characteristic of voluntary acts in primates. Preparatory neural activity preceding voluntary movements has been shown to be involved in movement planning (Kaufman et al, 2010) and decision making in primates (Steinmetz and Moore, 2010;Churchland et al, 2011). In Gymnotus sp., the higher sensory sampling rates during movement may be attributed to the increased demands on the brain to process the high flow of sensory information induced by selfmotion (Nelson and MacIver, 2006).…”

Weight-Specific Anticipatory Coding of Grip Force in Human Dorsal Premotor Cortex

“…A recent electrophysiological study in two monkeys supports the notion that inhibitory processes in PMd might prevail during motor preparation (Kaufman et al, 2010). Extracellular recordings were obtained from chronically implanted multielectrode arrays in contralateral PMd while monkeys performed a visuospatially instructed delayed reach task.…”