Elsevier

NeuroImage

Volume 65, 15 January 2013, Pages 52-58
NeuroImage

Two brakes are better than one: The neural bases of inhibitory control of motor memory traces

https://doi.org/10.1016/j.neuroimage.2012.09.048Get rights and content

Abstract

Inhibitory control of actions is one important aspect in daily life to warrant adequate context related behavior. Alpha activity (oscillatory brain activity around 10 Hz) has been suggested to play a major role for the implementation of inhibitory control. In the present study electrophysiological correlates of voluntary suppression of acquired, memorized motor actions have been compared to the suppression of novel motor actions. Multichannel EEG analyses of alpha power and alpha phase coherence were used. Healthy subjects were asked to inhibit the execution of either well-trained, memorized or untrained, novel sequential finger movements depending on the respective context. An increase of focal upper alpha activity at bilateral sensorimotor cortices was found during suppression of movements independent of whether these were memorized or novel. This represents a memory unspecific mechanism of motor cortical inhibition. In contrast, interregional phase synchronization between frontal and (left) central recording sites showed a differential effect with decoupling during suppression of memorized movements which was not the case with novel ones. Increase of fronto-central coupling at upper alpha frequency during retrieval of the memory trace and decrease during suppression of retrieval were obtained. This further supports the view of the functional relevance of upper alpha oscillations as a mechanism of context-dependent sustained inhibition of memory contents.

Highlights

► Neural bases of sustained voluntary suppression of complex movements were investigated. ► Memory unspecific control of movements by local EEG alpha amplitude over motor areas. ► Memory specific control of motor acts by fronto-central alpha phase synchronization.

Introduction

To act successfully in daily life the execution of well-trained motor skills has to be persistently withheld under certain circumstances. There are situations in which relatively complex sequential movements have to be performed due to a cue in the regular context. However, if the context has changed the movement might have to be voluntarily suppressed for at least a few seconds to act successfully, although the respective cue has appeared. For instance, while dining in a restaurant usually a guest takes the spoon and starts eating (motor program) after the waiter has put the soup (cue) on the table in front of the guest. If, however, the waiter tells the guest who has got intolerance to shellfish that the soup contains shrimps (changed context) the person has to inhibit starting to eat to prevent negative aftermath. During sustained voluntary inhibition of complex motor programs, i.e. the suppression of movements without any time constraints, a pattern of increased rhythmical brain activity around 10 Hz (so called alpha activity) was demonstrated in the human electroencephalogram (EEG) at recording sites overlying the motor cortex (Hummel et al., 2002). Increased alpha activity was associated with attenuated cortico-spinal excitability determined directly by transcranial magnetic stimulation (Hummel et al., 2002, Sauseng et al., 2009a, Sauseng et al., 2009b) and with a negative blood oxygenation level-dependent signal compared to unconstrained rest at motor areas (Hummel et al., 2004). These findings are well in line with the idea that high EEG alpha amplitudes are rather the neural signature of deactivation/inhibition of a cortical area (Klimesch et al., 2007) beyond simple nil-working or idling (Pfurtscheller et al., 1996).

An important question which still has remained open is whether increased EEG alpha activity during voluntary suppression of actions is restricted to acquired, memorized actions. Or in other words, is increased rhythmical brain activity in the alpha frequency range a neural correlate of action suppression in general or solely involved in the control of well-trained motor programs, i.e. actions that are stored in long-term memory? Following Keele et al. (1995) there are two different coding systems for movement sequences: an effector-based system in which muscle combinations are selected to code for sequences and an effector-free spatial coding system (or motor vs. cognitive coding scheme; Shea et al., 2011). Complex, novel actions which have not been performed before are likely to be coded effector-based. Well-trained movements, on the other hand, seem to be coded by an effector-free spatial representation system in addition to effector-based coding. So, if these two different types of actions (novel vs. well trained) are likely to be coded differently, it is also plausible that inhibitory control of these actions is implemented in two different ways. Whereas well-trained movements are most likely prepared as a complete and effector-free spatial representation which then is inhibited, for a novel motor program each digit of the sequential movement is effector-based represented and needs to be inhibited separately.

There is sound evidence for the assumption that inhibition of a motor memory trace (which would be an effector-free spatial representation) is associated with increased alpha activity (Hummel et al., 2002). It has been suggested that for instance during encoding and retention of information in working memory increased alpha activity can be found (Jensen et al., 2002, Klimesch et al., 1999, Sauseng et al., 2009a, Sauseng et al., 2009b). This indicates inhibition of task irrelevant brain areas (Jensen et al., 2002, Jokisch and Jensen, 2007, Klimesch et al., 1999, Sauseng et al., 2009a, Sauseng et al., 2009b) preventing the processing of distracting sensory information. It has also been discussed that high alpha activity reflects the top-down control of memory processes (Klimesch et al., 2007, Palva and Palva, 2007, Sauseng et al., 2005). Since this type of inhibitory activation is predominately found during memory processes inhibition of motor-related brain activity by the means of increased EEG alpha amplitude is expected particularly when there is a memory representation of a movement which has to be suppressed.

On the other hand, a recent study suggests that the voluntary suppression of a memory trace is associated with decreased distributed interregional coherence in the alpha frequency range (Bäuml et al., 2008). Bäuml et al. (2008) demonstrated a decrease of mainly temporal phase coherence at alpha frequency when participants attempted to deliberately inhibit information from episodic long-term memory. Moreover, interregional phase coherence might more likely reflect motor memory components of complex finger movements than local amplitude estimates (Sauseng et al., 2007). Thus, it is expected that interregional phase coherence at alpha frequency can dissociate between inhibition of memorized, well-trained movements and inhibition of novel motor programs.

To test whether the suppression of a motor memory trace is specifically reflected by focal increases of alpha power or decreases of interregional alpha phase coherence, multichannel EEG was recorded while subjects either had to perform or suppress well-trained or novel complex finger sequences depending on the respective context. Brain oscillatory activity was analyzed with an emphasis on amplitude estimate and phase coherence differences between the experimental conditions.

Section snippets

Material and methods

Twelve healthy volunteers participated in the study (7 female). Mean age was 26.6 ± 2.9 years (mean ± SD). Only volunteers who did not regularly play the piano were included in this protocol as musical (piano) education might possibly alter the way subjects learn complex finger movements. All subjects were right-handed according to the Edinburgh-Handedness-Scale and gave written informed consent according to the declaration of Helsinki (World Medical Association, 1996). The study protocol was

Behavioral results

Performance in the conditions requiring execution of sequences was close to ceiling. In the MEMORIZEDexecute condition accuracy of responses was at 92.8% (standard error of mean 1.4), and accuracy for NOVELexecute was at 96.1% (standard error of mean 0.7). A paired-sample t-test comparing these two conditions indicates that the difference is not statistically significant (t11 = 2.09, p = .06).

Task-related power

The two-way ANOVAs comprising the factors ACT (execute vs. suppress sequence) and MEMORY (memorized vs.

Discussion

Strong evidence has been provided that oscillatory EEG activity at alpha frequency reflects a cortical mechanism of suppression or deactivation of cortical areas (for a review see Klimesch et al., 2007). In the present study voluntary suppression of complex finger movements was associated with increased upper alpha power over the sensorimotor cortex compared to unconstraint rest, whereas there was upper alpha power reduction during movement execution. Importantly, these patterns are comparable,

Conclusion

Our data suggest that connectivity in a distributed cortical network is increased during execution of memorized sequences but attenuated during suppression. The distinction between local upper alpha activity and interregional phase coherence at upper alpha frequency helps dissociating two different neural mechanisms of context-dependent behavioral control, i.e. inhibitory control required by a cued change of environmental context.

Acknowledgments

This research was supported by the Austrian Science Fund FWF (Project P 22084-B18).

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