Altered processing of corollary discharge in thalamic lesion patients
Christian Bellebaum,1,4 Klaus-Peter Hoffmann,2,4 Benno Koch,3 Michael Schwarz3 and Irene Daum1,4
Institute of Cognitive Neuroscience, Department of Neuropsychology, Faculty of Psychology and Department of GeneralZoology and Neurobiology, Ruhr-University of Bochum, D-44780 Bochum, Germany 3 Department of Neurology, Klinikum Dortmund, Dortmund, Germany 4 International Graduate School of Neuroscience, Bochum, Germany Keywords: event-related potentials, posterior parietal cortex, saccades, updating
Accumulating evidence suggests that thalamic nuclei relay corollary discharge information ofsaccadic eye movements, enabling the visual system to update the representation of visual space. The present study aimed to explore the effect of thalamic lesions in humans on updating-related cortical processing. Event-related potentials were recorded while four patients with impairments in using corollary discharge information and 12 healthy control subjects performed a saccadic double-step task. Inthe experimental condition, which required the use of corollary discharge information, control subjects showed a pronounced positivity over the parietal cortex starting about 150 ms after ﬁrst saccade onset, reﬂecting the updating process. In the patients, parietal processing related to updating was altered. Three patients showed evidence of reduced updating event-related potential effects,consistent with a unilateral deﬁcit in using corollary discharge information. In two patients, the event-related potential topography differed signiﬁcantly from the topography pattern observed in controls. Thalamic damage affects updating-related processing, presumably due to insufﬁcient transfer of saccade-related information to parietal areas. This study thus provides further evidence for thalamicinvolvement in relaying corollary discharge information related to saccadic eye movements. Our data suggest that integration of corollary discharge and motor information occurs directly before the second saccade in a double-step task.
Whenever we perform a saccadic eye movement, the retinal positions of objects in our environment change. To achieve a stable percept of the world, visualspace must be updated. Thus, the retinal consequences of saccades must be accounted for by extraretinal signals, i.e. most probably corollary discharge signals of the motor command to move the eyes (Sperry, 1950; von Holst & Mittelstaedt, 1950). In monkeys, the medio-dorsal nucleus of the thalamus (MD) relays information about contralaterally directed saccades from the superior colliculus to thefrontal eye ﬁeld (FEF) (Sommer & Wurtz, 2004a,b). In humans, impairments in updating visual space have been found following lesions in the central thalamus (Gaymard et al., 1994), including the nuclei of the internal medullary lamina, and lesions in the centro-medial thalamus (Versino et al., 2000). In a more recent study, a large population of thalamic lesion patients differing in lesionlocations was studied using a saccadic double-step task (Bellebaum et al., 2005a) to assess the ability to use corollary discharge information of saccadic eye movements (Hallett & Lightstone, 1976). MD lesions as well as lateral thalamic lesions, involving the ventrolateral nucleus of the thalamus (VL), were associated with visual space-updating impairments, with deﬁcits after lateral lesions resemblingthose found in monkeys with MD lesions (Sommer & Wurtz, 2004b; Bellebaum et al., 2005a). In monkeys and humans, the posterior parietal cortex (PPC) has been shown to play an important role in integrating visual and saccade-related information (Duhamel et al., 1992a; Haarmeier et al., 1997; Heide & Kompf, 1998; Colby & Goldberg, 1999; Heide et al., 2001; Tobler et al., 2001; Medendorp et al.,...