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
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).
References (58)
- et al.
Neural dynamics of reaching following incorrect or absent motor preparation
Neuron
(2014) - et al.
Horse-race model simulations of the stop-signal procedure
Acta Psychologica
(2003) - et al.
The small scale functional topology of movement control: Hierarchical organization of local activity anticipates movement generation in the premotor cortex of primates
Neuroimage
(2020) - et al.
Controlled movement processing: Evidence for a common inhibitory control of finger, wrist, and arm movements
Neuroscience
(2012) - et al.
Cognitive control of movement in Down syndrome
Research in Developmental Disabilities
(2011) - et al.
Physiological markers of motor inhibition during human behavior
Trends in Neurosciences
(2017) - et al.
Arkypallidal cells send a stop signal to striatum
Neuron
(2016) - et al.
Dissociated multi-unit activity and local field potentials: A theory inspired analysis of a motor decision task
Neuroimage
(2010) - et al.
Antagonistic but not symmetric regulation of primary motor cortex by basal ganglia direct and indirect pathways
Neuron
(2015) - et al.
Proactive and reactive control of movement are differently affected in Attention Deficit Hyperactivity Disorder children
Research in Developmental Disabilities
(2013)
Stimulation of the dorsal premotor cortex, but not of the supplementary motor area proper, impairs the stop function in a STOP signal task
Neuroscience
Neural and behavioral correlates of selective stopping: Evidence for a different strategy adoption
Neuroimage
Deliberation and commitment in the premotor and primary motor cortex during dynamic decision making
Neuron
From reactive to proactive and selective control: Developing a richer model for stopping inappropriate responses
Biological Psychiatry
Converging evidence for a fronto-basal-ganglia network for inhibitory control of action and cognition
The Journal of Neuroscience
Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans
Nature Neuroscience
Frontosubthalamic circuits for control of action and cognition
The Journal of Neuroscience
Cortical and subcortical contributions to stop signal response inhibition: Role of the subthalamic nucleus
The Journal of Neuroscience
Selective stopping? Maybe not
Journal of Experimental Psychology General
The role of stimulus salience and attentional capture across the neural hierarchy in a stop-signal task
Plos One
A proactive mechanism for selective suppression of response tendencies
The Journal of Neuroscience
Functional dissociation in right inferior frontal cortex during performance of go/no-go task
Cerebral Cortex
Neural population dynamics during reaching
Nature
Dissociating the role of prefrontal and premotor cortices in controlling inhibitory mechanisms during motor preparation
The Journal of Neuroscience
Structure in neural population recordings: An expected byproduct of simpler phenomena?
Nature Neuroscience
Postsaccadic activities in the posterior parietal portex of primates are influenced by both eye movement vectors and eye position
The Journal of Neuroscience
Neuronal activity in the premotor cortex of monkeys reflects both cue salience and motivation for action generation and inhibition
bioRxiv
Role of frontal eye field in countermanding saccades: Visual, movement and fixation activity
Journal of Neurophysiology
A new emotional stroop-like task: Application to the down syndrome population
Archives of Clinical Neuropsychology
Cited by (14)
The effect of task complexity on the neural network for response inhibition: An ALE meta-analysis
2024, Neuroscience and Biobehavioral ReviewsThe role of dorsal premotor cortex in joint action stopping
2021, iScienceCitation Excerpt :In fact, single neuron activity in the monkey left dorsal premotor (lPMd) cortex integrates representations of self and others' actions, enabling successful coordination between individuals (Ferrari-Toniolo et al., 2019). Furthermore, previous studies in the macaque (Giarrocco et al., 2020; Mirabella et al., 2011) and human (Parmigiani and Cattaneo, 2018) have shown that PMd, but not other frontal areas connected to PMd (i.e., supplementary motor area [SMA] and pre-SMA; see also Friehs et al., 2021; Scangos and Stuphorn, 2010), plays a distinctive role in processing inhibitory signals during visuomotor inhibitory behavior. However, whether PMd regulates JA in general and JA stopping in particular has not been explored in humans yet.
The role of dorsal premotor cortex in joint action inhibition
2024, Scientific Reports