The role of the human thalamus in processing corollary discharge

Abstract

Corollary discharge signals play an important role in monitoring self-generated movements to guarantee spatial constancy. Recent work in macaques suggests that the thalamus conveys corollary discharge information of upcoming saccades passing from the superior colliculus to the frontal eye field. The present study aimed to investigate the involvement of the thalamus in humans by assessing the effect of thalamic lesions on the processing of corollary discharge information. Thirteen patients with selective thalamic lesions and 13 healthy age-matched control subjects performed a saccadic double-step task in which retino-spatial dissonance was induced, i.e. the retinal vector of the second target and the movement vector of the second saccade were different. Thus, the subjects could not rely on retinal information alone, but had to use corollary discharge information to correctly perform the second saccade. The amplitudes of first and second saccades were significantly smaller in patients than in controls. Five thalamic lesion patients showed unilateral deficits in using corollary discharge information, as revealed by asymmetries compared with the other patients and controls. Three patients with lateral thalamic lesions including the ventrolateral nucleus (VL) were impaired contralaterally to the side of damage and one patient with a lesion in the mediodorsal thalamus (MD) was impaired ipsilaterally to the lesion. The largest asymmetry was found in a patient with a bilateral thalamic lesion. The results provide evidence for a thalamic involvement in the processing of corollary discharge information in humans, with a potential role of both the VL and MD nuclei.

Human thalamus contributes to perceptual stability across eye movements

“…The systematic distortion of transsaccadic space integration matched the pattern of oculomotor planning deficits observed in our patient and in nonhuman primates after transient pharmacological inactivation of homologous thalamic regions (13). Our study thus significantly extends previous findings in nonhuman primates (13) and in patients with thalamic lesions (14) by showing that deficient internal monitoring signals indeed affect perceptual stability across eye movements.…”

“…The affected portions of central thalamus closely correspond to homologous portions of primate thalamus in which saccade-and eye positionrelated signals have been recorded previously (13,17). Although single lesions affecting the thalamus are occasionally encountered in larger cohorts of stroke patients (18), oculomotor abnormalities and other neurological and cognitive deficits are observed in the vast majority of these patients (14,19). Screening of the medical records and imaging databases in our department (>2,000 stroke patients/year) yielded no further subjects with unilateral lesions of similar selectivity in our thalamic region of interest.…”

“…Indeed, electrophysiological work in primates indicates that corollary discharge-related activity at the thalamic level represents both ipsi-and contralateral saccades and eye positions (17,29). Patient studies using a double-step task noted contra-and bilateral impairments with thalamic lesions but also strictly ipsilateral deficits in several cases (14,30). The observed lateralization of N.P.…”

“…Pharmacological inactivation studies in nonhuman primates (13) and lesion studies in humans (14) point to an involvement of this pathway in the planning of eye movement sequences. Inactivation studies furthermore demonstrated that predictive remapping of visual responses in the frontal eye fields relies on the integrity of these pathways (15).…”

“…Correct execution of the second saccade then depends on an internal estimate of the first saccade metrics (13,14,20). We compared the oculomotor performance in this condition with a control condition (VISUAL), in which no internal monitoring information was required for the correct execution of the saccade sequence (SI Experimental Procedures and Fig.…”