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, 29 (5), 931-42

Involvement of the Subthalamic Nucleus in Engagement With Behaviourally Relevant Stimuli

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Involvement of the Subthalamic Nucleus in Engagement With Behaviourally Relevant Stimuli

Paul Sauleau et al. Eur J Neurosci.

Abstract

In this study we investigate how the basal ganglia (BG) may process the behavioural relevance of environmental cues by recording local field potentials (LFPs) in the subthalamic nucleus of patients with Parkinson's disease who had undergone implantation of electrodes for deep brain stimulation. Fourteen patients were recorded as they performed a paradigm dissociating warning cue presentation from programming related to execution of specific tasks. Target and non-target warning cues of differing behavioural relevance were contrasted, and we evaluated if warning cue-evoked activities varied according to whether the eventual task to be performed was motor or cognitive and whether patients were receiving or withdrawn from dopaminergic therapy. Warning cues evoked a complex temporal sequence of activities with three epochs over the 760 ms following the onset of the warning cue. In contrast to the initial evoked LFP, evoked activities over two later periods were significantly influenced by behavioural relevance and by treatment state. The early activity was likely related to the initial orientating of attention induced by a novel target, while the delayed responses in our paradigm may reflect processing related to the non-motor resource implications of cues. The results suggest that the BG are intimately involved in the evaluation of changes in the environment and of their behavioural significance. The latter process is partly modulated by dopamine. Weakness in this function might contribute to the behavioural impairment that can follow BG lesions and surgery.

Figures

Fig. 1
Fig. 1
Schematic of two trials during the standard motor task. In this block type, patients were asked to copy the movement indicated by the body schema only when preceded by a circle. In the task, the body part to move was indicated in red. A similar sequence was used in the counting task.
Fig. 2
Fig. 2
Averaged LFP activity from right STN in patient 1 during the standard motor task. Signals were averaged around the warning circle cue (thin continuous vertical line at time=0 s), and are shown before (A) and after (B) z-transformation and conversion to absolute values. The vertical dashed line indicates a latency of 300 ms after the cue. Averages have been smoothed using a moving average filter with a period of 30 data points.
Fig. 4
Fig. 4
Mean amplitudes and standard deviation of the first (A), second (B) and third (C) activity periods Off (left column) and On (right column) medication for the target (circle, shown first) and non-target (square/triangle, shown second) warning cues in the standard moving and counting tasks. The solid line represents the difference in amplitude between ‘circle’ and ‘square/triangle’ in the standard motor task. The dashed line represents the same difference in amplitude for the counting task.
Fig. 3
Fig. 3
Grand averaged evoked potentials to target and non-target warning cues in the standard motor task (left column), control motor task (middle column) and counting (right column) task. (A) Off medication. The first panel represents the signals (mean ± SEM) evoked by target, the second panel represents the signal evoked by non-target, and the third panel represents the trace resulting from the subtraction of the two signals and the significant differences (P<0.05) between the signals evoked by the target and non-target cues sustained over=3 consecutive data points. (B) As above for On medication. Warning cue onset=0 s. Thick and thin dashed vertical lines represent the limits of activity periods 2 and 3, [340–500] and [600–760] ms after the warning cue onset, respectively. Grand averages have been smoothed using a moving average filter with a period of 30 data points.
Fig. 3
Fig. 3
Grand averaged evoked potentials to target and non-target warning cues in the standard motor task (left column), control motor task (middle column) and counting (right column) task. (A) Off medication. The first panel represents the signals (mean ± SEM) evoked by target, the second panel represents the signal evoked by non-target, and the third panel represents the trace resulting from the subtraction of the two signals and the significant differences (P<0.05) between the signals evoked by the target and non-target cues sustained over=3 consecutive data points. (B) As above for On medication. Warning cue onset=0 s. Thick and thin dashed vertical lines represent the limits of activity periods 2 and 3, [340–500] and [600–760] ms after the warning cue onset, respectively. Grand averages have been smoothed using a moving average filter with a period of 30 data points.
Fig. 5
Fig. 5
Distribution of the LFP amplitude during the first (A), second (B) and third (C) activity periods normalized to the contact pair with the maximum amplitude from each electrode (in the standard motor task). Negative values indicate polarity inversion relative to the sign of the contact pair with the maximum amplitude (defined as +100%).

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