Daniela Sochůrková

Cognitive potentials in the basal ganglia—frontocortical circuits. An intracerebral recording study

We studied cognitive functions related to processing sensory and motor activities in the basal ganglia (BG), specifically in the putamen and in cortical structures forming the BG-frontocortical circuits. Intracerebral recordings were made from 160 brain sites in 32 epilepsy surgery candidates. We studied P3-like potentials in five different tests evoked by auditory and visual stimuli, and two sustained potentials that are related to cognitive activities linked with movement preparation: BP (Bereitschaftspotential) and CNV (contingent negative variation). We compared the presence of a potential with a phase reversal or an amplitude gradient to the absence of a generator. All of the studied cognitive potentials were generated in the BG; the occurrence in frontal cortical areas was more selective. The frequency of all but one potential was significantly higher in the BG than in the prefrontal and in the cingulate cortices. The P3-like potentials elicited in the oddball paradigm were also more frequent in the BG than in the motor/premotor cortex, while the occurrence of potentials elicited in motor tasks (BP, CNV, and P3-like potentials in the CNV paradigm) in the motor cortex did not significantly differ from the occurrence in the BG. The processing of motor tasks fits with the model by Alexander et al. of segregated information processing in the motor loop. A variable and task-dependent internal organisation is more probable in cognitive sensory information processing. Cognitive potentials were recorded from all over the putamen. The BG may play an integrative role in cognitive information processing.

Intracerebral recording of cortical activity related to self-paced voluntary movements: a Bereitschaftspotential and event-related desynchronization/synchronization. SEEG study

To analyze the distribution of the cortical electrical activity related to self-paced voluntary movements, i.e. the movement-related readiness potentials (Bereitschaftspotential, BP) and the event-related desynchronization (ERD) and synchronization (ERS) of cortical rhythms using intracerebral recordings. EEG was recorded in 14 epilepsy surgery candidates during preoperative video-stereo-EEG monitoring. Subjects performed self-paced hand movements, with their right and left fingers in succession. EEG signals were obtained from a total of 501 contacts using depth electrodes located in primary and nonprimary cortical regions. In accordance with previous studies, BP was found consistently in the primary motor (M1) and somatosensory (S1) cortex, the supplementary motor area (SMA), and in a few recordings also in the cingulate cortex and in the dorsolateral prefrontal and premotor cortex. ERD and ERS of alpha and beta rhythms were also observed in these cortical regions. The distribution of contacts showing ERD or ERS was larger than the distribution of those showing BP. In contrast to BP, ERD and ERS frequently occurred in the lateral and mesial temporal cortex and the inferior parietal lobule. The number of contacts and cortical regions showing ERD and ERS and not BP suggests that the two electrophysiological phenomena are differently involved in the preparation and execution of simple voluntary movements. Substantial differences between BP and ERD in spatial distribution and the widespread topography of ERD/ERS in temporal and higher-order motor regions suggest that oscillatory cortical changes are coupled with cognitive processes supporting movement tasks, such as memory, time interval estimation, and attention.

Cognitive‐ and movement‐related potentials recorded in the human basal ganglia

Sources of potentials evoked by cognitive processing of sensory and motor activities were studied in 9 epilepsy surgery candidates with electrodes implanted in the basal ganglia (BG), mostly in the putamen. Several contacts were also located in the pallidum and the caudate. The recorded potentials were related to a variety of cognitive and motor activities (attentional, decisional, time estimation, sensory processing, motor preparation, and so on). In five different tests, we recorded P3‐like potentials evoked by auditory and visual stimuli and sustained potential shifts in the Bereitschaftspotential and Contingent Negative Variation protocols. All of the studied potentials were generated in the BG. They were recorded from all over the putamen. Various potentials on the same lead or nearby contacts were recorded. A functional topography in the BG was not displayed. We presume that the cognitive processes we studied were produced in clusters of neurons that are organized in the basal ganglia differently than the known functional organization, e.g., of motor functions. The basal ganglia, specifically the striatum, may play an integrative role in cognitive information processing, in motor as well as in nonmotor tasks. This role seems to be nonspecific in terms of stimulus modality and in terms of the cognitive context of the task.

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

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.