We continuously move our eyes when we inspect a visual scene. Although this leads to a rapid succession of discontinuous and fragmented retinal snapshots, we perceive the world as stable and coherent. Neural mechanisms underlying visual stability may depend on internal monitoring of planned or ongoing eye movements. In the macaque brain, a pathway for the transmission of such signals has been identified that is relayed by central thalamic nuclei. Here, we studied a possible role of this pathway for perceptual stability in a patient with a selective lesion affecting homologous regions of the human thalamus. Compared with controls, the patient exhibited a unilateral deficit in monitoring his eye movements. This deficit was manifest by a systematic inaccuracy both in successive eye movements and in judging the locations of visual stimuli. In addition, perceptual consequences of oculomotor targeting errors were erroneously attributed to external stimulus changes. These findings show that the human brain draws on transthalamic monitoring signals to bridge the perceptual discontinuities generated by our eye movements.saccade | corollary discharge | efference copy | extraretinal
Internal monitoring of oculomotor commands may help to anticipate and keep track of changes in perceptual input imposed by our eye movements. Neurophysiological studies in non-human primates identified corollary discharge (CD) signals of oculomotor commands that are conveyed via thalamus to frontal cortices. We tested whether disruption of these monitoring pathways on the thalamic level impairs the perceptual matching of visual input before and after an eye movement in human subjects. Fourteen patients with focal thalamic stroke and 20 healthy control subjects performed a task requiring a perceptual judgment across eye movements. Subjects reported the apparent displacement of a target cue that jumped unpredictably in sync with a saccadic eye movement. In a critical condition of this task, six patients exhibited clearly asymmetric perceptual performance for rightward vs. leftward saccade direction. Furthermore, perceptual judgments in seven patients systematically depended on oculomotor targeting errors, with self-generated targeting errors erroneously attributed to external stimulus jumps. Voxel-based lesion-symptom mapping identified an area in right central thalamus as critical for the perceptual matching of visual space across eye movements. Our findings suggest that trans-thalamic CD transmission decisively contributes to a correct prediction of the perceptual consequences of oculomotor actions.
Previous patient studies suggest that thalamic stroke may yield persistent deficits in several cognitive domains. At present, the subjective dimension and everyday relevance of these impairments is unclear, since many patients with thalamic stroke only show minor changes on physical examination. Here, we have studied subjective consequences of focal thalamic lesions. A sample of 68 patients with a history of ischemic thalamic stroke was examined by using established clinical self-report questionnaires assessing memory, attention, executive functions, emotional status and health-related quality of life. In order to control for general factors related to cerebrovascular disease, self-reports were compared to an age-matched group of 34 patients with a history of transient ischemic attack. Thalamic lesions were co-registered to an atlas of the human thalamus. Lesion overlap and subtraction analyses were used for lesion-to-symptom mapping. When both patient groups were compared, no significant differences were found for either questionnaire. However, when subgroups were compared, patients with infarctions involving the posterior thalamus showed significant emotional disturbances and elevated anxiety levels compared to patients with more anterior lesions. Our findings thus point to the existence of a persistent affective impairment associated with chronic lesions of the posterior thalamus. This syndrome may result from damage to connections between medial pulvinar and extra-thalamic regions involved in affective processing. Our findings suggest that the posterior thalamus may contribute significantly to the regulation of mood.
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