Neuronal population dynamics during motor plan cancellation in nonhuman primates

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.

Response inhibition in premotor cortex corresponds to a complex reshuffle of the mesoscopic information network

“…Conversely, there was no significant difference in spiking activity between the Go and wrong Stop trials at any of the sites. A similar trend was found in all recording sessions (Table S1), confirming previous findings on the role of PMd in inhibitory motor control and the relevance of the epoch of analysis in motor decisions in Stop trials 20, 22–24, 76–79 . This level of analysis, however, does not provide information on how the nodes in the investigated network interacted.…”

“…Overall recording sessions (ses Table S1), there was a significant modulation of the SA sampled every 400 micrometers across the three behavioral conditions of the task, thus confirming previous observations on the involvement of PMd in inhibitory motor control and of the relevance of the epoch following the Stop signal appearance - in Stop trials - when decisions are taken 15, 16, 24–29 . However, at this stage, other than the heterogeneity of different modules in relation to the task, nothing could be inferred about the structure of the information transfer, the functional relationship between different modules, and the collective state of the network at the moment of the motor decision.…”

“…Along these lines, the state recorded during a wrong Stop, being topologically relatable to that of a correct Stop and, at the same time, showing the same patterns of information transfer of Go trials, would result from an erroneous transmission of the inhibitory coding, probably due to a persistent strong recruitment of the Go_drivers and a contemporary weaker involvement of the Stop_drivers, as it happens during Go trials. This is in agreement with what we described in one of our recent papers in which we analyzed the dynamics of neural activity in the same task with a state-space approach 29 . Indeed, in such a scenario, we demonstrated how a subspace in which neural activities are confined before movement generation and during movement suppression exists.…”

“…Some studies have employed the Stop signal task 19 , that requires actively inhibiting an upcoming movement upon presentation of a Stop signal, to investigate how neuronal activity in this area supports both movement generation and cancellation. According to these studies, neuronal activity in PMd is strongly related to both the generation and the suppression of an arm movement at different scales, from single neurons 20, 21 to population of neurons 22 and local mesoscopic signals 14, 23, 24 .…”

Reward prospect affects strategic adjustments in stop signal task

“…This requires, for example, assessing the potential reward that could be obtained in a specific context before deciding whether or not to act, and being able to stop quickly if sudden changes in the environment make the action no longer useful. A widely used experimental paradigm to study choice behavior is the Stop-Signal Task (SST) in both human and non-human primates (Vince, 1948;Logan and Cowan, 1984;Hanes and Carpenter, 1999;Scangos and Stuphorn, 2010;Brunamonti et al, 2012;Pani et al, 2014;Montanari et al, 2017;Schall et al, 2017;Pani et al, 2018;Bardella et al, 2020;Fiori et al, 2020;Giarrocco et al, 2021;Andujar et al, 2022;Hervault et al, 2022;Pani et al, 2022;Bardella et al, 2023;Marc et al, 2023). The SST requires the subjects to respond as quickly as possible when a Go Signal is presented (for example by pressing a button) and to interrupt the response when unpredictably a Stop Signal is presented after a variable time from the Go Signal.…”