Supplementary Motor Area Exerts Proactive and Reactive Control of Arm Movements

Abstract

Adaptive behavior requires the ability to flexibly control actions. This can occur either proactively to anticipate task requirements, or reactively in response to sudden changes. Here we report neuronal activity in the supplementary motor area (SMA) that is correlated with both forms of behavioral control. Single-unit and multiunit activity and intracranial local field potentials (LFPs) were recorded in macaque monkeys during a stop-signal task, which elicits both proactive and reactive behavioral control. The LFP power in high-(60 -150 Hz) and low-(25-40 Hz) frequency bands was significantly correlated with arm movement reaction time, starting before target onset. Multiunit and single-unit activity also showed a significant regression with reaction time. In addition, LFPs and multiunit and single-unit activity changed their activity level depending on the trial history, mirroring adjustments on the behavioral level. Together, these findings indicate that neuronal activity in the SMA exerts proactive control of arm movements by adjusting the level of motor readiness. On trials when the monkeys successfully canceled arm movements in response to an unforeseen stop signal, the LFP power, particularly in a low (10 -50 Hz) frequency range, increased early enough to be causally related to the inhibition of the arm movement on those trials. This indicated that neuronal activity in the SMA is also involved in response inhibition in reaction to sudden task changes. Our findings indicate, therefore, that SMA plays a role in the proactive control of motor readiness and the reactive inhibition of unwanted movements.

The role of the right presupplementary motor area in stopping action: two studies with event-related transcranial magnetic stimulation

“…In functional magnetic resonance imaging (fMRI) studies, activation in the right preSMA (and usually also the anterior cingulate) is greater on trials for which participants successfully cancel a prepotent response compared with trials for which they do not (Aron and Poldrack 2006;Aron et al 2007a;Boecker et al 2010;Boehler et al 2010;Cai and Leung 2009;Chevrier et al 2007;Chikazoe et al 2009b;Curtis et al 2005;Hampshire et al 2010;Sharp et al 2010). Neurophysiologic studies have also shown activation in the preSMA prior to and during stopping (Chen et al 2010;Swann et al 2012). Several studies with macroelectrode stimulation in epilepsy patients show that preSMA stimulation leads to the arrest of ongoing vocal or manual movements (Luders et al 1988;Mikuni et al 2006;Swann et al 2012).…”

Attention to baseline: does orienting visuospatial attention really facilitate target detection?

“…Such cue-related response inhibition probably involves multiple executive and motor mechanisms (Duque et al 2010;Stinear et al 2009;Van Der Lubbe et al 2005). Importantly, this inhibitory control relies not only on postcue responsive mechanisms but also on precue proactive mechanisms that depend on the subject's expectations of the trial structure (Jaffard et al 2007Boulinguez et al 2008Boulinguez et al , 2009Boy et al 2010;Chen et al 2010). A major consequence of this is that these proactive mechanisms influence the neutral cue condition, whenever one is set up to measure attentional effects, leading to possible misinterpretations of classical behavioral outcomes ( Fig.…”

Foresight beats hindsight: The neural correlates underlying motor preparation in the pro‐/anti‐cue paradigm

“…The role of pre‐SMA in proactive motor preparation was repeatedly emphasized in research on animals (Fujii, Mushiake, & Tanji, 2002; Halsband, Matsuzaka, & Tanji, 1994) and humans (Chen et al., 2010; Jaffard et al., 2008; Stuphorn & Emeric, 2012; Wardak, 2011). It was especially shown to be causally relevant to the organization of action sequences (Kennerley, Sakai, & Rushworth, 2004).…”

“…According to Aron (2011), proactive elements of motor behavior are very prominent in everyday life, even suggesting that the dynamic interaction of proactive and reactive processes underpins almost all real‐life motor actions. Not focusing on the neural correlates of proactive and reactive processes compromises the “ecological validity” of findings (Aron, 2011; Chen, Scangos, & Stuphorn, 2010; Jaffard et al., 2008; Verbruggen, Adams, & Chambers, 2012). Yet, to study such mechanisms in the brain, one requires a robust behavioral paradigm that reliably triggers proactive processes.…”

“…This is not straightforward given the complexity of influences on motor behavior: For example, proactive inhibitory control varies with context, depending on exogenous and endogenous cues, expectations, and implicit temporal structures in the surroundings (Wardak, Ramanoël, Guipponi, Boulinguez, & Ben Hamed, 2012). While neuroscientific research on proactive control is still in its infancy, a growing number of studies explores the role of various brain regions, such as pre‐supplementary motor area (pre‐SMA), in proactive motor control (Chen et al., 2010; Jaffard et al., 2008; Stuphorn & Emeric, 2012; Wardak, 2011). …”