Elsevier

Clinical Neurophysiology

Volume 116, Issue 8, August 2005, Pages 1879-1888
Clinical Neurophysiology

Lateralization of event-related beta desynchronization in the EEG during pre-cued reaction time tasks

https://doi.org/10.1016/j.clinph.2005.03.017Get rights and content

Abstract

Objective

Here, we investigate whether the event-related desynchronization (ERD) of spectral components of the cortical EEG in the beta (13–30 Hz) frequency range may, in part, index motor selection processes. Specifically, we sought evidence for a contralaterally dominant component of the beta ERD that is limited to trials in which motor selection is possible prior to any imperative cue to move, with attendant behavioural advantage.

Methods

We measured reaction time and assessed the lateralization of beta ERD in 12 healthy volunteers as they performed pre-cued choice reaction time tasks, in which warning S1 cues were either fully predictive about the laterality of a subsequent imperative S2 signal or provided no laterality information. We calculated ‘lateralized ERD index’ (LERDI), a parallel measure to the lateralized readiness potential in the time domain.

Results

Trials with 100% S1–S2 congruency produced significantly shorter reaction times than trials with 50% S1–S2 congruency, where laterality information was unreliable. Beta LERDI indicated significantly greater lateralisation of the ERD in the warning-go interval and of event-related synchronization (ERS) following movement in the 100% condition than in the 50% condition. The lateralization of the beta ERD with respect to hand persisted, even when subjects were instructed to make movements of opposite laterality to those prompted.

Conclusions

Lateralized EEG changes occur in the beta band in the S1–S2 interval prior to movement, but only when informative warning cues allow early motor selection, as suggested by the shortening of reaction time. Furthermore, the enhanced contralateral ERS with 100% S1–S2 congruency suggests that this phenomenon is at least partly independent of afferent feedback, as the same movement was made in the 100 and 50% conditions.

Significance

Lateralized suppression of beta power prior to externally generated movements is associated with motor selection.

Introduction

Voluntary movements are preceded by a variety of EEG activities, believed to be related to motor preparation. In particular, the predominance of these activities contralateral to subsequent movements has been considered important evidence of a relationship between these EEG features and motor preparation. In the time domain, self-paced movements are preceded by a slow negative potential termed the Bereitschaftspotential (Kornhuber and Deeke, 1965), larger at scalp sites contralateral to upper limb movements (Ikeda and Shibasaki, 1992, Lang et al., 1994, Vaughn et al., 1968). Pre-cued movements are also preceded by a negative potential, the contingent negative variation (CNV), first described by Walter et al. (1964). This too is bigger contralateral to the ensuing movement (Kutas and Donchin, 1980), as evidenced by the lateralized readiness potential (De Jong et al., 1988, Gratton et al., 1988, Wauschkuhn et al., 1997). The latter is obtained by subtracting activity at an EEG electrode ipsilateral to the movement from that at the corresponding contralateral electrode, separately for left and right movements and then obtaining an average of the two differences.

More recently, attention has turned to spectral features in the EEG preceding movement, as these reflect ongoing changes in one or more parameters that control oscillations in neural networks, rather than transient post-synaptic responses of main pyramidal neurons triggered by and phase-locked to a specific stimulus (Pfurtscheller and Lopes da Silva, 1999). Typically, self-paced voluntary hand movements are preceded by a decrease in the power of oscillatory EEG activities in the beta frequency band over central cortical areas (Pfurtscheller, 1981, Pfurtscheller and Lopes da Silva, 1999, Pfurtscheller et al., 2003, Szurhaj et al., 2003). This phenomenon, known as event-related desynchronization (ERD), is then followed by event-related synchronisation (ERS) within the first second of the movement. The ERD is believed to indicate a state of active cortical processing (Gerloff et al., 1998, Leocani et al., 2001, Pfurtscheller and Lopes da Silva, 1999, Szurhaj et al., 2003). Accordingly, the beta ERD is larger contralateral to self-paced movement, becoming bilateral during movement execution (Manganotti et al., 1998, Pfurtscheller and Lopes da Silva, 1999, Leocani et al., 2001, Pfurtscheller et al., 2003, Szurhaj et al., 2003). On the other hand, the beta ERS has been postulated to be involved in the termination of movement (Salmelin et al., 1995), or to be a consequence of movement related afferent feed-back (Cassim et al., 2000, Cassim et al., 2001). However, the latter is contentious, since beta synchrony has also been observed after imagined movements (Pfurtscheller et al., 1997, Pfurtscheller and Lopes da Silva, 1999, Pfurtscheller, 2000) and no-go cues (Leocani et al., 2001).

A contralateral beta ERD has also been described prior to triggered movements but after stimulus presentation (Kaiser et al., 2001, Kaiser et al., 2003, Leocani et al., 2001), or prior to imperative stimuli delivered with high temporal predictability (Alegre et al., 2003). The pre-movement ERD recorded under these circumstances could reflect a number of processes such as overt or covert shifts in attention, and motor preparative processes related to when and what to move. Here, we determine whether there is evidence to suggest that part of the pre-movement beta ERD may specifically relate to motor selection processes (what to move). To this end we used the paradigm described in detail by Williams et al., 2003, Williams et al., 2005, in which warning S1 cues are either fully predictive about the laterality of a subsequent imperative S2 signal or provide no laterality information. In this setting, trials with 100% S1–S2 congruency with respect to laterality have shorter reaction times than trials with 50% S1–S2 congruency that provide no laterality information. The predictability of the timing of the movement (when to move) is kept unchanged across 100 and 50% S1–S2 congruency trials by maintaining a fixed S1–S2 interval. We reasoned that motor selection processes should be greater over the hemisphere contralateral to the responding limb and only become lateralized during the S1–S2 interval in trials with 100%, as opposed to 50% S1–S2 congruency, as only in the former case it is possible to prepare movement related to a specific limb. In trials with 50% S1–S2 congruency motor selection processes in the S1–S2 interval are necessarily bilateral, if they occur at all. In addition, we reasoned that lateralization of the ERS in trials with 100%, as opposed to 50% S1–S2 congruency would provide further evidence that the ERS is at least partly independent of afferent feedback, as the same movement is made in each case. This experimental approach was combined with the assessment of a lateralized ERD index (LERDI) in the beta band, a parallel measure to the lateralized readiness potential in the time domain. Finally, to exclude the possibility that any contralateral dominance of the beta ERD in the S1–S2 interval might be due to overt or covert shifts in visuospatial attention rather than motor selection, we also instructed some of our subjects to move the hand contralateral to the side indicated by the imperative S2 cue. In this situation, motor preparative activity should be maximal contralateral to the hand movement, but activity related to shifts in visual attention should be greater ipsilateral to the hand movement.

Section snippets

Subjects

Experiments were carried out on 12 right handed (Oldfield, 1971) healthy subjects (age 33±7 years, 6 males). All volunteers gave informed consent, and the study was approved by the joint ethics committee of the Institute of Neurology and National Hospital for Neurology and Neurosurgery, in accordance with The Code of Ethics of the World Medical Association (Declaration of Helsinki, 1967).

Behavioural task

Subjects were instructed to fixate on a cross at the centre of a portable PC screen while holding a

Behavioural data

All subjects, except one, displayed a longer reaction time in the 50% condition than the 100% condition. Incorrect and premature responses accounted for 0.25±0.52 and 0.22±0.47%, respectively, of the total number of trials performed. In a 2×2 repeated measures analysis of variance (ANOVA) of reaction times, there was a main effect for probability level (F[1,11]=51.2, P<0.001), but not for the hand used (F[1,11]=0.8, P=0.38). Post-hoc two-tailed paired t-test confirmed that reaction times were

Discussion

The results of this study provide strong support for the hypothesis that the lateralized pre-movement beta band ERD in cued two-choice response tasks indexes motor selection processes that depend on the context set by the warning cue and which offer behavioural advantage through their early implementation. We found that the LERDI in both the warning-imperative cue interval and post-cue period was significantly greater in trials with 100% as opposed to 50% warning-imperative cue congruency,

Conclusion

The current study provides further evidence that suppression of oscillatory beta activity in the EEG relates, at least in part, to the preparation of functionally appropriate motor responses, particularly motor selection. Thus, lateralization of the ERD only occurred under conditions allowing subjects to accurately pre-plan forthcoming movements. The enhanced lateralization of the beta ERS under similar circumstances suggests that it is related to recovery processes following the preceding ERD

Acknowledgements

This work was funded by the MRC.

References (66)

  • W. MacKay

    Synchronized neuronal oscillations and their role in motor processes

    Trends Cogn Sci

    (1997)
  • P. Manganotti et al.

    Task-related coherence and task related spectral power changes during sequential finger movements

    Electroenceph Clin Neurophysiol

    (1998)
  • R.C. Oldfield

    The assessment and analysis of handedness: the Edinburgh inventory

    Neuropsychologia

    (1971)
  • R. Oostenveld et al.

    Overlap of attentional and movement-related activity in lateralized event-related brain potentials

    Clin Neurophysiol

    (2001)
  • A. Osman et al.

    Temporal organization of covert motor processes during response selection and preparation

    Biol Psychol

    (2003)
  • G. Pfurtscheller

    Central beta rhythm during sensorimotor activities in man

    Electroencephalogr Clin Neurophysiol

    (1981)
  • G. Pfurtscheller

    Event-related synchronization (ERS): an electrophysiological correlate of cortical areas at rest

    Electroencephalogr Clin Neurophysiol

    (1992)
  • G. Pfurtscheller

    Spatiotemporal ERD/ERS patterns during voluntary movement and motor imagery

    Suppl Clin Neurophysiol

    (2000)
  • G. Pfurtscheller et al.

    Evaluation of event-related desynchronization (ERD) preceding and following voluntary self-paced movement

    Electroencephalogr Clin Neurophysiol

    (1979)
  • G. Pfurtscheller et al.

    Event-related EEG/MEG synchronization and desynchronization: basic principles

    Clin Neurophysiol

    (1999)
  • G. Pfurtscheller et al.

    Post-movement beta synchronization. A correlate of an idling motor area?

    Electroencephalogr Clin Neurophysiol

    (1996)
  • G. Pfurtscheller et al.

    EEG-based discrimination between imagination of right and left hand movement

    Electroencephalogr Clin Neurophysiol

    (1997)
  • G. Pfurtscheller et al.

    Spatiotemporal patterns of beta desynchronization and gamma synchronization in corticographic data during self-paced movement

    Clin Neurophysiol

    (2003)
  • R. Salmelin et al.

    Spatiotemporal characteristics of sensorimotor neuromagnetic rhythms related to thumb movement

    Neuroscience

    (1994)
  • R. Salmelin et al.

    Functional segregation of movement-related rhythmic activity in the human brain

    Neuroimage

    (1995)
  • T. Shibata et al.

    Event-related dynamics of the gamma-band oscillation in the human brain: information processing during a GO/NOGO hand movement task

    Neurosci Res

    (1999)
  • A. Stancák et al.

    Desynchronization and recovery of β rhythms during brisk and slow self-paced finger movements in man

    Neurosci Lett

    (1995)
  • W. Szurhaj et al.

    Basic mechanisms of central rhythms reactivity to preparation and execution of a voluntary movement: a stereoencephalographic study

    Clin Neurophysiol

    (2003)
  • G.W. Thickbroom et al.

    Premotor negaticity associated with saccadic eye movement and finger movement: a comparative study

    Brain Res

    (1990)
  • D. Van't Ent et al.

    Inter-hemispheric lateralization of event-related potentials; motoric versus non-motoric cortical activity

    Electroencephalogr Clin Neurophysiol

    (1998)
  • E. Wascher et al.

    The interaction of stimulus- and response-related process measured by event-related lateralizations of the EEG

    Electroencephalogr Clin Neurophysiol

    (1996)
  • B. Wauschkuhn et al.

    Lateralized cortical activity due to preparation of saccades and finger movements: a comparative study

    Electroenceph Clin Neurophysiol

    (1997)
  • M. Alegre et al.

    Alpha and beta oscillatory changes during stimulus-induced movement paradigms: effect of stimulus predictability

    Neuroreport

    (2003)
  • Cited by (131)

    • Cueing brain rhythms in Parkinson's disease

      2021, Clinical Neurophysiology
    View all citing articles on Scopus
    View full text