Intracerebral ERD/ERS in voluntary movement and in cognitive visuomotor task

Abstract

In order to study cerebral activity related to preparation and execution of movement, evoked and induced brain electrical activities were compared to each other and to fMRI results in voluntary self-paced movements. Also, the event-related desynchronization and synchronization (ERD/ERS) were studied in complex movements with various degrees of cognitive load. The Bereitschaftspotential (BP) and alpha (8–12 Hz) and beta (16–24 Hz) ERD/ERS rhythms in self-paced simple movements were analyzed in 14 epilepsy surgery candidates. In previous studies, the cortical sources of BP were consistently displayed contralateral to the movement in the primary motor cortex and somatosensory cortex, and bilateral in the supplementary motor area (SMA) and in the cingulate cortex. There were also small and inconstant BP generators in the ipsilateral sensorimotor, premotor, and dorsolateral prefrontal cortex. Alpha and beta ERD/ERS were also observed in these cortical regions. The distribution of contacts showing ERD or ERS was larger than of those showing BP. In contrast to BP, ERD, and ERS frequently occurred in the orbitofrontal, lateral and mesial temporal cortices, and inferior parietal lobule. The spatial location of brain activation for self-paced repetitive movements, i.e., writing simple dots, was studied using event-related functional MRI (fMRI) in 10 healthy right-handed subjects. We observed significant activation in regions known to participate in motor control: contralateral to the movement in the primary sensorimotor and supramarginal cortices, the SMA and the underlying cingulate, and, to a lesser extent, the ipsilateral sensorimotor region. When the fMRI was compared with the map of the brain areas electrically active with self-paced movements (intracerebral recordings; Rektor et al., 1994, 1998, 2001b, c; Rektor, 2003), there was an evident overlap of most results. Nevertheless, the electrophysiological studies were more sensitive in uncovering small active areas, i.e., in the premotor and prefrontal cortices. The BP and the event-related hemodynamic changes were displayed in regions known to participate in motor control. The cortical occurrence of oscillatory activities in the alpha–beta range was clearly more widespread. Four epilepsy surgery candidates with implanted depth brain electrodes performed two visuomotor-cognitive tasks with cued complex movements: a simple task — copying randomly presented letters from the monitor; and a more complex task — writing a letter other than that which appears on the monitor. The second task demanded an increased cognitive load, i.e., of executive functions. Alpha and beta ERD/ERS rhythms were evaluated. Similar results for both tasks were found in the majority of the frontal contacts, i.e., in the SMA, anterior cingulate, premotor, and dorsolateral prefrontal cortices. The most frequent observed activity was ERD in the beta rhythm; alpha ERS and ERD were also present. Significant differences between the two tasks appeared in several frontal areas — in the dorsolateral and ventrolateral prefrontal and orbitofrontal cortices (BA 9, 45, 11), and in the temporal neocortex (BA 21). In several contacts localized in these areas, namely in the lateral temporal cortex, there were significant changes only with the complex task — mostly beta ERD. Although the fMRI results fit well with the map of the evoked activity (BP), several discrepant localizations were displayed when the BP was compared with the distribution of the oscillatory activity (ERD-ERS). The BP and hemodynamic changes are closely related to the motor control areas; ERD/ERS represent the broader physiological aspects of motor execution and control. The BP probably reflects regional activation, while the more widespread ERD/ERS may reflect the spread of task-relevant information across relevant areas. In the writing tasks, the spatial distribution of the alpha–beta ERD/ERS in the frontal and lateral temporal cortices was partially task dependent. The ERD/ERS occurred there predominantly in the more complex of the writing tasks. Some sites were only active in the task with the increased demand on executive functions. In the temporal neocortex only, the oscillatory, but not the evoked, activity was recorded in the self-paced movement. The temporal appearance of changes of oscillatory activities in the self-paced movement task as well as in the cued movement task with an increased load of executive functions raises the interesting question of the role of this region in cognitive-movement information processing.

Introduction

What do brain rhythms tell us? Nearly 80 years after their first description by Hans Berger, this question remains largely unanswered, despite the immense progress achieved during the last decades. The oscillations linked with various functions, e.g., with attention, have been studied extensively in humans as well as in animals. The work by Pfurtscheller's group in particular has answered a number of questions in the field of the motor control and cognition (Pfurtscheller and Lopes da Silva 1999; Kamp et al., 2005). The studies performed in Pfurtscheller's laboratory opened the door to a better understanding of the motor functions on the one hand, and of the nature of brain rhythmical activity on the other. Nevertheless, the physiological and behavioral activities expressed by the oscillations are still not completely understood, although the biophysical processes producing the oscillations at the neuronal level are quite well known ( Llinás et al., 2005). Evoked activities such as the Bereitschaftspotential (BP) or the P300 have been studied more extensively, and their physiological meanings have been widely and variously interpreted. By comparing the cerebral locations of the task-related changes in oscillatory activities, evoked activities, and cerebral perfusion, we attempt to resolve some of the questions raised by these changes. We present the results of three intracerebral studies, complemented by an fMRI study. We studied the brain activity linked with preparation and execution of self-paced movements using three methods — the event-related desynchronization and synchronization (ERD/ERS), the BP, and the fMRI. We then focused on brain oscillation induced by a complex cognitive-motor task with an increased demand on executive function.

Four sections are presented as follows:

• The cerebral location of ERD/ERS and BP in the self-paced movement paradigm.

• The cerebral location of blood oxygen level-dependent (BOLD) effect (fMRI) in the self-paced movement paradigm.

• The fronto-lateral temporal location of ERD/ERS related to writing of single letters and to the executive functions.

• Conclusion.

In the electrophysiological studies, intracerebral recordings were performed (stereoelectroencephalography, SEEG). Subdural recordings were used only in some cases. Intracranial recordings may help to answer the questions raised in this chapter. There are medical reasons for human subjects to have electrode contacts that record subcortically and from the cortex. When the electrodes are placed, it is possible for the depth electrodes to provide direct information from cortical and subcortical structures. Intracerebral recordings can provide information not readily available through other means. Intracerebral recording reveal the multidimensionality of the neuronal responses, which consists of event-related evoked potentials, induced desynchronization, and synchronization in distinct frequency bands (Brovelli et al., 2005). The changes of BOLD effect provide information complementary to the electrophysiological studies — the methods will be reported in the section “The fronto-lateral temporal location of ERD/ERS related to writing of single letters and to the executive functions.”

The candidates for epilepsy surgery were patients who had remained unresponsive to conventional forms of therapy, and who were recommended by a special commission for stereotactic exploration. A neuropsychological examination excluded severe cognitive disturbances and dementia in each patient. All the patients had normal hearing, and normal or corrected-to-normal vision. Consent was obtained from each patient for the electrophysiological testing, about which they were amply informed. The local ethics committee approved the experiment.

Each patient received 6–12 orthogonal platinum electrodes in the investigated brain structures according to the methodology by Talairach and Bancaud (1973). Microdeep (DIXI Besançon) intracerebral 5–15 contact stainless steel and later platinum electrodes were used. The electrode diameter was 0.8 mm, the contact length was 2 mm, and the distance between contacts was 1.3 mm.The electrodes were implanted stereotactically. For subdural recordings, radionics platinum electrode strips and grids were used. The position of the electrodes was verified by MRI, and their functionality was verified by electrical stimulation. The video-SEEG (stereoelectroencephalographic) recordings were performed over a period of 5–10 days. Regions with clearly pathological SEEG activity or MRI lesions were excluded from further evaluations.

The data acquisition and averaging in the first BP studies were performed using Nihon Kohden Neuropack 4 and 8 set, the band was 0.01–500 Hz for the intracerebral recordings. The BP and ERD/ERS recordings were performed with a 96-channel M&I neurophysiological device, and later with the 128 channel EEG system TruScan (Alien Technic). The recordings were monopolar, with a linked earlobe reference. The sampling rate was 256 Hz.Standard anti-aliasing filters were used. The EMG (m. flexor carpi radialis), the EOG, and the scalp EEG (Cz, Pz, and Fz electrodes) were generally recorded simultaneously.

For averaged potentials the absolute amplitudes were measured from the baseline. The distance from the electrode to the generator heavily influences the amplitude of intracerebrally recorded potentials, and thus the differences of amplitude can only be compared intraindividually. The intracerebral potentials occurred with both positive and negative polarities. This was due to variances in the positions of the electrode contact and the dipole generator.

Our results could be biased by two phenomena typical of intracerebral studies. The first is the low spatial resolution of intracerebral recordings. This is compensated in our studies by the high number of recording sites in the regions of interests. The intracranial explorations in human subjects are targeted according to clinical data, and thus some regions remained insufficiently explored. The second possible bias is the fact that our recordings were performed in epileptic patients. Although the recordings from epileptic tissue were excluded from evaluations, there still remains the question of the possible influence of cortical excitability in subjects with epilepsy. This possibility cannot be fully excluded, but a previous ERD study showed normal alpha-ERD over the perirolandic area in patients with temporal lobe epilepsy (Derambure et al., 1997). The influence of epilepsy on the presence of ERD and ERS in the temporal lobe is also improbable because our recordings were obtained from the temporal lobe ipsilateral as well as contralateral to the epileptogenic zone, and no difference was observed.