Abstract
The oculomotor role of the basal ganglia has been supported by extensive evidence, although their role in scanning eye movements is poorly understood. Nineteen Parkinsońs disease patients, which underwent implantation of deep brain stimulation electrodes, were investigated with simultaneous intraoperative microelectrode recordings and single channel electrooculography in a scanning eye movement task by viewing a series of colored pictures selected from the International Affective Picture System. Four patients additionally underwent a visually guided saccade task. Microelectrode recordings were analyzed selectively from the subthalamic nucleus, substantia nigra pars reticulata and from the globus pallidus by the WaveClus program which allowed for detection and sorting of individual neurons. The relationship between neuronal firing rate and eye movements was studied by crosscorrelation analysis. Out of 183 neurons that were detected, 130 were found in the subthalamic nucleus, 30 in the substantia nigra and 23 in the globus pallidus. Twenty percent of the neurons in each of these structures showed eye movement-related activity. Neurons related to scanning eye movements were mostly unrelated to the visually guided saccades. We conclude that a relatively large number of basal ganglia neurons are involved in eye motion control. Surprisingly, neurons related to scanning eye movements differed from neurons activated during saccades suggesting functional specialization and segregation of both systems for eye movement control.
Highlights
In everyday life we scan the environment with a series of eye movements, pointing the fovea towards objects of interest and the most salient areas of the scene
We have focused on the subthalamic nucleus (STN), substantia nigra pars reticulata (SNr) and globus pallidus (GP) – i.e. nuclei in which eye movements (EM)-related activity was previously reported [11,13] and which are accessible during the implantation procedure for deep brain stimulation in Parkinsons disease (PD)
Neuronal activity related to scanning eye movements Thirty seven (20%) out of 183 neurons identified in the basal ganglia during the scanning EM task were related to at least one of the EM kinematic parameters (POS, VELOC, ACCEL) (Table 3)
Summary
In everyday life we scan the environment with a series of eye movements, pointing the fovea towards objects of interest and the most salient areas of the scene. The pattern of such eye movements (EM) carried out while exploring an image, called scanning EM, is composed of a succession of small saccades and fixations, corresponding to successive re-allocation of attention from one detail to another [1,2]. An involvement of the basal ganglia during scanning EM was suggested by early research using regional cerebral blood flow in healthy controls and schizophrenic patients [7]. The only evidence of human EM-related neurons was obtained from the subthalamic nucleus during saccade tasks and smooth pursuit movements in patients with Parkinson’s disease [21]
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