Elsevier

Cortex

Volume 135, February 2021, Pages 326-340
Cortex

Special Issue “The Brain’s Brake: Inhibitory Mechanisms in Cognition and Action”
Neuronal dynamics of signal selective motor plan cancellation in the macaque dorsal premotor cortex

https://doi.org/10.1016/j.cortex.2020.09.032Get rights and content

Abstract

Primates adopt various strategies to interact with the environment. Yet, no study has examined the effects of behavioural strategies with regard to how movement inhibition is implemented at the neuronal level. We used a modified version of the stop-task by adding an extra signal – termed the Ignore signal – capable of influencing the inhibition of movements only within a specific strategy. We simultaneously recorded multisite neuronal activity from the dorsal premotor (PMd) cortex of macaque monkeys during the task and applied a state-space 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 behavioural strategy is adopted. Moreover, neuronal signatures during the inhibitory process were predictive of how PMd processes inhibitory signals, allowing the classification of the resulting behavioural strategy. Our data further corroborate the PMd as a critical node in movement inhibition.

Introduction

Primates have the crucial ability to suppress actions rapidly, a capacity that can be strategically regulated. For example, they can decide to delay an on-going action if something occurs suddenly in the environment: this momentary pause could allow them to better evaluate the consequence of the action and decide their next move. Alternatively, they can choose to ignore the new signal and continue pursuing the initial goal.

Neuroscience studies have typically examined simple forms of movement inhibition in experimental settings, using the stop (or countermanding) task (Hanes, Patterson, & Schall, 1998; Logan & Cowan, 1984). In this task, the primary instruction is to respond as quickly as possible to a Go signal; in a minority of trials a Stop signal is presented after the Go signal, and subjects are required to refrain from moving. The ability to countermand the response is evaluated, based on the estimate of the stop signal reaction time (SSRT). The SSRT can be broadly considered to be the response time of movement inhibition (Logan & Cowan, 1984) and as such has been used to compare the efficiency of inhibitory control in various populations of patients; during the many stages of brain maturation, from childhood to senescence; and across animal species (Brunamonti et al., 2011; Brunamonti, Ferraina, & Paré, 2012; Hanes et al., 1998; Hippolyte, Iglesias, & Barisnikov, 2009; Lijffijt, Kenemans, Verbaten, & van Engeland, 2005; Lipszyc & Schachar, 2010; Pani et al., 2013; Pani et al., 2014; Paré & Hanes, 2003; Williams, Ponesse, Schachar, Logan, & Tannock, 1999). However, because inhibition can intervene to regulate behaviour in many ways, in recent years, more complex tasks have been used to determine the behavioural consequences of and the neuronal functional architecture that underlies complex inhibitory control (Aron, 2010; Bissett & Logan, 2014; Boehler, Appelbaum, Krebs, Chen, & Woldorff, 2011; Cai, Oldenkamp, & Aron, 2011; Chikazoe et al., 2009; Majid, Cai, George, Verbruggen, & Aron, 2012; Sebastian et al., 2016, 2017; Sharp et al., 2010; Xu et al., 2017; Xu, Mayse, & Courtney, 2018). Among the tasks that have been proposed, the selective stop task (Bissett & Logan, 2014) entails the presentation of a Stop signal or an Ignore signal after the Go signal in a subset of trials, of which only the Stop signal requires inhibition of the movement.

Behavioural studies in humans (Bissett & Logan, 2014; Sánchez-Carmona, Albert, & Hinojosa, 2016; Sebastian et al., 2017) demonstrated that subjects are able to deal with the task successfully, suppressing the action only when required. Bissett and Logan (2014), first suggested that some subjects adopt the strategy to activate the inhibitory control momentarily procrastinating the discrimination between proposed signals while other subjects adopt the strategy to first discriminate then respond/stop as necessary. Conclusions were based on behavioural evidence only.

In the present study we evaluated the presence of a neuronal correlate of the strategy adopted in monkeys trained in the selective stop task.

Among the different areas involved in the inhibitory control of planned actions, both at the cortical and subcortical levels (Cai et al., 2011; Aron et al., 2007; Wessel & Aron, 2017; Aron & Poldrack, 2006; Aron, Fletcher, Bullmore, Sahakian, & Robbins, 2003; Wagner, Wessel, Ghahremani, & Aron, 2018; Duque, Labruna, Verset, Olivier, & Ivry, 2012; Duque, Greenhouse, Labruna, & Ivry, 2017; Parmigiani & Cattaneo, 2018; Hanes et al., 1998, Pare'& Hanes, 2003; Schmidt, Leventhal, Mallet, Chen, & Berke, 2013; Mallet et al., 2016), we focused on the dorsal premotor cortex (PMd), an area crucial in establishing the transition from decision to action for arm movements; neuronal activity in PMd continuously reflects the accumulation and change in information that is pertinent to the momentary decision state regarding forthcoming movements (Kaufman, Churchland, Ryu, & Shenoy, 2014; Thura & Cisek, 2014), and predicts when and whether an arm movement will be generated or inhibited (Kaufman et al., 2016; Mirabella, Pani, & Ferraina, 2011; Pani et al., 2014, 2018).

By analysing the multisite dynamics of neuronal activity in the PMd, we obtained evidence of a strategy-dependent inhibitory neuronal process, triggered by the Ignore signal only when monkeys adopted a specific strategy. These novel data corroborate the model proposed by Bissett and Logan (2014) in humans and demonstrate, once again, the strong correlation between modulation of the neuronal activity in the PMd and the adopted behaviour, suggesting PMd as a key structure in the cognitive control of movements.

Section snippets

Subjects

Two male rhesus macaque monkeys (Macaca mulatta; designated Monkeys 1 and 2), weighing 9 and 13 kg, were studied. We designed the study assuming sample sizes similar to those used in other monkey studies (see for example, Genovesio, Brunamonti, Giusti, & Ferraina, 2007; Pani et al., 2018). The monkeys were pair-housed with cage enrichment. They were fed daily with standard primate chow, supplemented with nuts and fresh fruits. The monkeys received part of their daily water supply during the

Behavioural results

We derived behavioural data from 15 sessions (see Table 1; Monkey 1, 10 sessions; Monkey 2, 5 sessions) with a sufficient number of trials for analysis.

We found that monkeys adopted either the DTS or the STD strategy on different days. Consistent with the independence assumption of the race model, in both strategies, the SSRT divides the distribution of RTs in no-signal trials (Fig. 2, A shows 2 sample sessions; 1 for each strategy for the same animal) for fast (left portion) and slow (right

Discussion

We examined the neuronal instantiation of inhibition in the PMd using a stimulus selective stop task. This task allowed us to determine the influence of the behavioural strategy on the processing of the Ignore signal.

We found that monkeys performed the selective stop task using 2 strategies—STD and DTS—while solving the ignore-signal trials and that there was a strong correlation between the adopted strategy and the effect of the Ignore signal. Specifically, an inhibitory effect on neuronal

Authors contribution

F.G., P.P, and S.F. designed the experiment. F.G., F.F. prepared the experimental setup and collected the data. F.G. and G.B. analyzed the data. All authors participated in the interpretation of data and helped draft the manuscript; P.P. and S.F. supervised the project. All authors gave final approval for publication.

Open practices

The study in this article earned Open Materials and Open Data badges for transparent practices. Materials and data for the study are available at: https://osf.io/qfs3k/.

We report how we determined our sample size, all data exclusions, all inclusion/exclusion criteria, whether inclusion/exclusion criteria were established prior to data analysis, all manipulations, and all measures in the study.

No part of the study procedures neither study analyses were pre-registered prior to the research being

Acknowledgments

We thank Jeff Schall and one anonymous reviewer for constructive comments to the first draft of the manuscript. Partially supported by Sapienza (grant number PH117IC823A9528, 2017).

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