Eye-head coordination in the guinea pig II. Responses to self-generated (voluntary) head movements

• Published in: Experimental brain research 2010-09, Vol.205 (4), p.445-454
• Main Authors: Shanidze, N, Kim, A. H, Loewenstein, S, Raphael, Y, King, W. M
• Format: Article
• Language: English
• Subjects: Animals; Anticipatory movements; Biological and medical sciences; Biomedical and Life Sciences; Biomedicine; Eye; Eye and associated structures. Visual pathways and centers. Vision; Eye movements; Eye Movements - physiology; Eye-hand coordination; Feed-forward models; Fundamental and applied biological sciences. Psychology; Gaze; Guinea Pigs; Head Movements - physiology; Motor control and motor pathways. Reflexes. Control centers of vegetative functions. Vestibular system and equilibration; Movements; Neurology; Neurosciences; Orientation - physiology; Physiological aspects; Psychomotor Performance - physiology; Reaction Time - physiology; Reflex, Vestibulo-Ocular - physiology; Research Article; Vertebrates: nervous system and sense organs; Vestibulo-ocular reflex
• ISSN: 0014-4819; 1432-1106
• DOI: 10.1007/s00221-010-2375-3

Retinal image stability is essential for vision but may be degraded by head movements. The vestibulo-ocular reflex (VOR) compensates for passive perturbations of head position and is usually assumed to be the major neural mechanism for ocular stability. During our recent investigation of vestibular reflexes in guinea pigs free to move their heads (Shanidze et al. in Exp Brain Res, 2010), we observed compensatory eye movements that could not have been initiated either by vestibular or neck proprioceptive reflexes because they occurred with zero or negative latency with respect to head movement. These movements always occurred in association with self-generated (active) head or body movements and thus anticipated a voluntary movement. We found the anticipatory responses to differ from those produced by the VOR in two significant ways. First, anticipatory responses are characterized by temporal synchrony with voluntary head movements (latency ~1 versus ~7 ms for the VOR). Second, the anticipatory responses have higher gains (0.80 vs. 0.46 for the VOR) and thus more effectively stabilize the retinal image during voluntary head movements. We suggest that anticipatory responses act synergistically with the VOR to stabilize retinal images. Furthermore, they are independent of actual vestibular sensation since they occur in guinea pigs with complete peripheral vestibular lesions. Conceptually, anticipatory responses could be produced by a feed-forward neural controller that transforms efferent motor commands for head movement into estimates of the sensory consequences of those movements.