No abstract

To understand the cortical neuronal dynamics behind movement generation and control, most studies have focused on tasks where actions were planned and then executed using different instances of visuomotor transformations. However, to fully understand the dynamics related to movement control, one must also study how movements are actively inhibited. Inhibition, indeed, represents the first level of control both when different alternatives are available and only one solution could be adopted and when it is necessary to maintain the current position. We recorded neuronal activity from a multielectrode array in the dorsal premotor cortex (PMd) of monkeys performing a countermanding reaching task that requires, in a subset of trials, them to cancel a planned movement before its onset. In the analysis of the neuronal state space of PMd, we found a subspace in which activities conveying temporal information were confined during active inhibition and position holding. Movement execution required activities to escape from this subspace toward an orthogonal subspace and, furthermore, surpass a threshold associated with the maturation of the motor plan. These results revealed further details in the neuronal dynamics underlying movement control, extending the hypothesis that neuronal computation confined in an “output-null” subspace does not produce movements.

The voluntary control of movement is often tested by using the countermanding, or stop-signal task that sporadically requires the suppression of a movement in response to an incoming stop-signal. Neurophysiological recordings in monkeys engaged in the countermanding task have shown that dorsal premotor cortex (PMd) is implicated in movement control. An open question is whether and how the perceptual demands inherent the stop-signal affects inhibitory performance and their underlying neuronal correlates. To this aim we recorded multi-unit activity (MUA) from the PMd of two male monkeys performing a countermanding task in which the salience of the stop-signals was modulated. Consistently to what has been observed in humans, we found that less salient stimuli worsened the inhibitory performance. At the neuronal level, these behavioral results were subtended by the following modulations: when the stop-signal was not noticeable compared to the salient condition the preparatory neuronal activity in PMd started to be affected later and with a less sharp dynamic. This neuronal pattern is probably the consequence of a less efficient inhibitory command useful to interrupt the neural dynamic that supports movement generation in PMd.

Primates adopt various strategies to interact with the environment. Yet, no study has examined the effects of behavioral strategies with regard to how movement inhibition is implemented at the neuronal level. We modified a classical approach to study movement control (stop-task) by adding an extra signal-termed the Ignore signal-which influenced movement inhibition only under a specific strategy. We simultaneously recorded multisite neuronal activity from the dorsal premotor (PMd) cortex of macaque monkeys during a task and applied a statespace approach. As a result, we found that movement generation is characterized by neuronal dynamics that evolve between subspaces. When the movement is halted, this evolution is arrested and inverted. Conversely, when the Ignore signal is presented, inversion of the evolution is observed briefly and only when a specific behavioral strategy is adopted. Moreover, neuronal signatures during the inhibitory process were predictive of how PMd processes inhibitory signals, allowing the classification of the resulting behavioral strategy. Our data corroborate the PMd as a critical node in movement inhibition. .

The connectivity among architectonically defined areas of the frontal, parietal, and temporal cortex of the macaque has been extensively mapped through tract tracing methods. To investigate the statistical organization underlying this connectivity, and identify its underlying architecture, we performed a hierarchical cluster analysis on 69 cortical areas based on their anatomically defined inputs. We identified 10 frontal, 4 parietal, and 5 temporal hierarchically related sets of areas (clusters), defined by unique sets of inputs and typically composed of anatomically contiguous areas. Across cortex, clusters that share functional properties were linked by dominant information processing circuits in a topographically organized manner that reflects the organization of the main fiber bundles in the cortex. This led to a dorsal-ventral subdivision of the frontal cortex, where dorsal and ventral clusters showed privileged connectivity with parietal and temporal areas, respectively. Ventrally, temporo-frontal circuits encode information to discriminate objects in the environment, their value, emotional properties, and functions such as memory and spatial navigation. Dorsal parieto-frontal circuits encode information for selecting, generating, and monitoring appropriate actions based on visual-spatial and somatosensory information. This organization may reflect evolutionary antecedents, in which the vertebrate pallium, which is the ancestral cortex, was defined by a ventral and lateral olfactory region and a medial hippocampal region.