Elsevier

Clinical Neurophysiology

Volume 111, Issue 10, 1 October 2000, Pages 1847-1859
Clinical Neurophysiology

High resolution spatiotemporal analysis of the contingent negative variation in simple or complex motor tasks and a non-motor task

https://doi.org/10.1016/S1388-2457(00)00388-6Get rights and content

Abstract

Objectives: Since the characteristics of the Bereitschaftspotential (BP) – voluntary movement paradigm of internally-driven movements – have been established recently by our group using high resolution DC-EEG techniques, it was of great interest to apply similar techniques to the other slow brain potential – contingent negative variation (CNV) of externally-cued movements – with the same motor tasks using the same subjects.

Methods: The CNV for simple bimanual sequential movements (task 1), complex bimanual sequential movements (task 2) and a non-motor condition (task 3) was recorded on the scalp using a 64 channel DC-EEG in 16 healthy subjects, and the data were analyzed with high resolution spatiotemporal statistics and current source density (CSD).

Results: (1) The CNV was distributed over frontal, frontocentral, central and centroparietal regions; a negative potential was found at the frontal pole and a positive potential was found over occipital regions. (2) CNV amplitudes were higher for task 2 than for task 1, and there was no late CNV for task 3. (3) A high resolution spatiotemporal analysis revealed that during the early CNV component, statistical differences existed between the motor tasks (tasks 1 and 2) and the non-motor task (task 3), which occurred at frontocentral, central, centroparietal, parietal and parieto-occipital regions. During the late CNV component, additional significant differences were found not only between the motor tasks and the non-motor task but also between motor task 1 and task 2 at frontocentral, central and centroparietal regions. (4) Comparison of the CNV between the frontomesial cortex (situated over the supplementary/cingulate areas, SCMA) and both lateral pre-central areas (situated over the primary motor areas, MIs) showed that there was no statistically significant difference between the two cortical motor areas except for the early CNV. (5) Comparison of the CNV between the 3 tasks over the cortical motor areas showed that there were significant differences between the motor tasks and the non-motor task regarding the auditory evoked potential (AEP) and the early CNV component, and between all 3 tasks in the late CNV, the visual evoked potential (VEP2) and the N-P component. (6) The ranges and the densities of the CSD maps were larger and higher for complex than for simple tasks. The current sinks of the AEP and the early CNV were located at Fz, the late CNV at FCz and surrounding regions. As to be expected, current sources of the VEPs were located at the occipital lobes. The CNV was a current sink (negative) except for the VEP's main component which was a current source (positive).

Conclusions: (1) The CNV topography over the scalp varied with the complexity of motor tasks and between motor and non-motor conditions. (2) The origin of the early CNV may rest in the frontal lobes, while the late CNV may stem from more extensive cortical areas including SCMA, MIs, etc. (3) The late CNV component is not identical with the BP.

Introduction

In our last paper we investigated the Bereitschaftspotential (BP, readiness potential) preceding voluntary bimanual simple and complex finger movement sequences at frontomesial and both lateral pre-central areas of the scalp situated over supplementary/cingulate or primary motor areas, respectively (SCMA or MIs), and found that not just the BP had a significantly higher amplitude for the complex than for the simple task, but statistically significant task differences prior to −0.96 s mainly appeared at frontomesial areas of the scalp (situated over the SCMA) rather than at either lateral pre-central area (situated over MI) (Cui et al., 2000). Furthermore, the BP had a significantly higher amplitude in SCMA than it had in the MIs. The current sinks of the current source density (CSD) map were always located at the frontocentral midline. This was so during the early component of the BP (BP1) and during the late component (BP2). These results supported the hypothesis that SCMA was involved in both early as well as late stages of self-initiation of a movement, SCMA playing a role of triggering and ‘supervising’ voluntary (internally-driven) movement, while the MIs were involved in the late stage of voluntary movement, playing the role of execution (Deecke et al., 1976, Deecke and Lang, 1996, Lang et al., 1991, Lang et al., 1994, Cui et al., 1996a, Cui et al., 1996b, Cui et al., 1999, Cui and Deecke, 1999).

It became of interest to investigate whether similar results would be found in another slow brain potential – contingent negative variation (CNV) occurring with externally-cued movements – or whether there are intrinsic differences between internally-driven movements (actions, BP paradigm) and externally-cued movements (re-actions, CNV paradigm). In other words, we wanted to know whether different sequential movement tasks that were shown to affect the BP also affect the CNV, and if so, whether there would be differences in topography, amplitude, CSD area, extension, etc?

The CNV was first described by Walter et al. (1964). It has been studied since in numerous experiments using different kinds of movements, e.g. left wrist extension (Ikeda et al., 1997), wrist flexion (Grünewald et al., 1979), thumb pressing of a key (Oishi et al., 1995), middle finger extension (Ikeda et al., 1994), middle finger and thumb abduction or dorsiflexion (Ikeda and Shibasaki, 1995, Ikeda et al., 1996), foot flexion or extension (Brunia and Dautzenberg, 1986), simple foot dorsiflexions (Yazawa et al., 1997), and push button with the right index finger (Hultin et al., 1996). However, no paper is available on the CNV paradigm with the present simple or complex bimanual sequential finger movements (tasks 1 and 2) as compared to non-motor (task 3).

In the CNV paradigm, evoked potentials (auditory, visual, etc.) are always intermingled with the motor responses, so that the generators of the CNV may well be different from that of the BP, which is free from external cues. Ikeda et al. (1996) stated that in humans orbitofrontal and mesial frontal areas play an important role in regard to cognition and decision making. Recently, these authors reported that subcortical generating mechanisms are also involved and are different for the late CNV and BP, although both may share some cortical generators, and what is more, that the basal ganglia are most likely responsible for the generation of the late CNV (Ikeda et al., 1997). Hultin et al. (1996) found that the dominant source of the late CNV was located near the bottom of the pre-central sulcus at the anterior bank of the pre-central gyrus, close to the superior frontal sulcus. They ventured that the late CNV may be closely related to the readiness potential, and that the major cortical activity is symmetrically located at the left and right pre-motor areas. Drake et al. (1997) advocate a frontal lobe generator for the CNV. Yazawa et al. (1997) reviewed the results of both humans and animals and hypothesized that some frontal areas, including the SMA and the MIs, were the generators of the late CNV. Hamano et al. (1997) pointed out that the CNV recorded from the scalp is the summation of multiple cortical potentials which have different origins and different functions. These are said to include orbitofrontal and mesial frontal areas (Ikeda et al., 1996), the MI, SMA, mesial, basal and lateral pre-frontal areas (Ikeda and Shibasaki, 1995), and the frontal lobe (Drake et al., 1997), so we are far away from a clear concept envisaging an exact generator of the CNV.

Attempts to find relationships between CNV and BP have focused on the late components of the two brain waves. One viewpoint regards the CNV, like the BP, as primarily related to response factors, and postulates hence that the CNV and the BP are essentially the same phenomenon (Grünewald et al., 1979, Rohrbaugh et al., 1976, Rohrbaugh et al., 1980, Prescott, 1986). But clinical studies found that in some patients with lesions in the cerebellum, the BP disappeared completely whereas the CNV remained as usual. In other patients with cerebellar lesions, the contrary was found. The BP remained normal, while the CNV was abnormal (Ikeda et al., 1994, Ikeda et al., 1997). Furthermore, in a CNV paradigm without a motor task in response to the second stimulus (S2), well-pronounced negativity is recorded prior to S2 (Ruchkin et al., 1986, Tecce and Cattanach, 1993). These results suggest that the CNV must be different from the BP. The third viewpoint regards the CNV as clearly different from the BP, although at least the late CNV may share generators with the BP, since using depth electrodes in monkeys or in patients with intractable epilepsy, the CNV could be recorded from pre-frontal, pre-motor, SMA, and MI areas (McSherry and Borda, 1973, Gemba et al., 1990, Lamarche et al., 1995, Hamano et al., 1997), areas that also contribute to the BP.

Systematic studies covering all cortical regions with multichannel scalp recordings and high resolution spatiotemporal analysis of the whole cortical electrophysiological message have not yet been carried out, although they are needed. Therefore, it was the aim of the present study to employ the 64 channel DC-EEG system for recording the cortical DC potential on the scalp in the CNV paradigm and to analyze the data with high spatiotemporal resolution statistics and the CSD technique.

The CNV paradigm has been associated with terms such as attention, cognition, judgement, estimation, determination, planning, preparation, expectancy and motor processing (Ikeda et al., 1996, Yazawa et al., 1997). For S1 and S2 various combinations have been selected, such as a pair of tone bursts (Ikeda et al., 1994, Ikeda et al., 1996, Ikeda et al., 1997, Hamano et al., 1997), a visual flash and a tone (Hultin et al., 1996), a click and a flash (Oishi et al., 1995), a tone and a flash (Rohrbaugh et al., 1976), or two tones (Grünewald et al., 1979). In the present experiment, in order to have enough time for judgement, determination, planning and preparation of the different movement tasks and to decrease the complex content of S1, another stimulus was placed before the traditional S1 and S2 stimuli, i.e. a pre-alerting stimulus (S0). S0 (eliciting visual evoked potential ‘VEP1’) was presented 1 s before S1 in order to warn and alert the subject to pay attention to S1 (which thus came second in the present paradigm, eliciting auditory evoked potential ‘AEP’). S1 provided information about which of the 3 tasks had to be performed upon S2 (classical choice reaction time paradigm). Finally came the classical ‘imperative stimulus’ S2 (eliciting ‘VEP2’), which was the command for the subject to execute that individual task – one out of 3 – which had just been announced by S1.

Section snippets

Subjects

Sixteen right-handed subjects (4 females, 12 males) ranging in age from 27 to 40 years (average 32.72±3.83) participated in the experiment. None of the them suffered from any neurological or mental disease. Hand dominance was assessed using an improved Oldfield's questionnaire (Cui et al., 1996b), and all subjects scored 100% dextrality.

Paradigm and tasks

Subjects received a sequence of 3 stimuli (S0, S1 and S2) in each trial (Fig. 1A). The first stimulus (S0), eliciting attention for S1, was the change of an

CNV topography, waveform and naming of components

Fig. 2 shows the topography of our present CNV paradigm potential complex with the simple, complex and non-motor tasks in the grand average mean of all subjects. Fig. 3I shows a high resolution waveform and the components of the present CNV paradigm: VEP1, AEP and VEP2.

The general distribution of the present CNV paradigm potential complex is shown in Fig. 2 (also cf. Fig. 3II). (a) Amplitudes of the present CNV paradigm potential complex were high at frontal (F), frontocentral (FC), central (C)

Discussion

After having extensively studied the BP topography using high resolution DC-EEG and CSD analysis (Cui et al., 1996a, Cui et al., 1996b, Cui et al., 1999, Cui et al., 2000, Cui and Deecke, 1999), it was of interest, using the same method, to investigate the CNV topography.

Acknowledgements

This work was supported by the Human Frontier Science Program (HFSP, Project: Brain dynamics of complex behaviour revealed by functional neuromagnetic imaging), and the Austrian Research Council (Fonds zur Förderung der Wissenschaftlichen Forschung, Project FWF P11437-MED and FWF P 12515-MED) (L.D.).

References (49)

  • A Ikeda et al.

    Dissociation between contingent negative variation (CNV) and Bereitschaftspotential (BP) in patients with parkinsonism

    Electroenceph clin Neurophysiol

    (1997)
  • H.H Kornhuber et al.

    Will, volitional action, attention and cerebral potentials in man: Bereitschaftspotential, performance-related potentials, directed attention potential, EEG spectrum changes

  • J.D Kropotov et al.

    Human depth ERP in a visual threshold recognition task

    Electroenceph clin Neurophysiol

    (1991)
  • M Lamarche et al.

    Intracerebral recordings of slow potentials in a contingent negative variation paradigm: in exploration in epileptic patients

    Electroenceph clin Neurophysiol

    (1995)
  • M Oishi et al.

    Contingent negative variation and movement-related cortical potentials in parkinsonism

    Electroenceph clin Neurophysiol

    (1995)
  • C Pantev et al.

    Identification of sources of brain neuronal activity with high spatiotemporal resolution through a combination of neuromagnetic source localization and magnetic resonance imaging

    Electroenceph clin Neurophysiol

    (1990)
  • P Praamstra et al.

    Dipole source analysis suggests selective modulation of the supplementary motor area contribution to the readiness potential

    Electroenceph clin Neurophysiol

    (1996)
  • R.L Rogers et al.

    Neuromagnetic evidence of a dynamic excitation pattern generating the N100 auditory response

    Electroenceph clin Neurophysiol

    (1990)
  • D.S Ruchkin et al.

    Terminal CNV in the absence of motor response

    Electroenceph clin Neurophysiol

    (1986)
  • G.J Van-Boxtel et al.

    Motor and non-motor aspects of slow brain potentials

    Biol Psychol

    (1994)
  • S Yazawa et al.

    Cortical mechanism underlying externally cued gait initiation studied by contingent negative variation

    Electroenceph clin Neurophysiol

    (1997)
  • Brunia CHM, Dautzenberg JEMW. Cortical potentials in man preceding a plantar flexion and dorsiflexion of the foot. In:...
  • R.Q Cui et al.

    High resolution DC-EEG analysis of the Bereitschaftspotential and post movement onset potentials accompanying uni- or bilateral voluntary finger movements

    Brain Topogr

    (1999)
  • R.Q Cui et al.

    Which parts of the cortex contribute to the Bereitschaftspotential? – analysis of current source densities (CSD) with a spherical head model

    Mov Disord

    (1996)
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