How the Brain Moves the Eyes and the Head

Saccadic Eye Movements

Modulation of Visual Processing by Saccades. Robert H. Wurtz, Kerry McAlonan, and James Cavanaugh

The modulation of visual processing by saccades is well established, and a classic paper by Buttner and Fuchs (1973) explored this modulation in the lateral geniculate nucleus (LGN), the major relay between the retina and visual cortex. A more subtle type of such saccadic modulation of LGN visual responses might accompany saccades in so far as neuronal activity associated with saccade generation has been proposed to underlie the enhanced visual responses accompanying visual spatial attention. We have investigated this attentional modulation in the LGN and its satellite nucleus, the thalamic reticular nucleus (TRN), by comparing the visual response when the monkey attends to the stimulus to the response when it attends elsewhere. We find increased initial visual responses with attention in both LGN magnocellular and parvocellular neurons, but decreased responses in TRN neurons. This is consistent with the TRN acting on the LGN through an inhibitory connection. Later visual activity in both divisions of the LGN also increases with attention. But there is no such change in the TRN neuronal activity, which suggests that this later visual attention effect results from inputs other than those from TRN. One or the other or both of these attentional modulations might well be produced by input from the saccadic system, particularly input from the superior colliculus.

Cerebellar Control of Gaze:

Changes in simple spike P-cell activity in the oculomotor vermis during saccade adaptation. Kojima Y, Soetedjo R, Fuchs AF

The oculomotor system gradually adjusts saccade size to reduce the error produced by persistent saccadic dysmetrias. During amplitude decrease adaptation, the activity of neurons in the caudal fastigial nucleus (cFN) of the cerebellum decreases with contraversive and increases with ipsiversive saccade amplitude. The cFN receives inhibitory projections from Purkinje (P-cells) in the cerebellar oculomotor vermis. Here we tested how the simple spike (SS) activity of P-cells that showed phasic discharges (pause, burst or combination) with saccades changed during adaptations.
Complex spikes (CS) of most saccade-related P-cells discharge best when an inaccurate saccade causes an error in a preferred (on) direction. If CSs report an error signal that drives saccade adaptation, SS activity also should be best modulated with adaptation in that direction. Therefore, we first determined the on direction of a unit’s CSs online and then adapted 25° saccades in that and the opposite (off) direction. We compared the SS activity at the beginning and end of adaptation.
After adaptation, SS activity of 14/24 P-cells showed either a shallower/shorter pause or a greater burst in the CS-off direction; either change would lead to increased cFN activity. 7/24 P-cells showed a deeper/longer pause or lower burst in the CS-on direction; both would lead to decreased cFN activity. Similar changes occurred neither for non-adapted saccades of the same size nor during the fatigue induced by repeated saccades.
These changes in P-cell activity are appropriate to influence neurons in the cFN in ways that could help produce the adapted, smaller saccades.

Coordination of Head and Eye Movements:

Coordination of eye and head movement following loss of modulated vestibular input from the semicircular canals. J.O. Phillips, L. Ling, S.D. Newlands, and A.F. Fuchs

Vestibular mechanisms have an important role in coordinating eye and head movement. However, following permanent loss of vestibular input, eye and head movement coordination is rapidly restored to produce accurate head unrestrained gaze shifts. Recordings from neurons in the brainstem of the rhesus monkey suggest that a new neural control strategy, emphasizing precise control of head and not eye movement, emerges to allow for accurate gaze.

The caudal fastigial nucleus and the control of gaze orientation : lessons from perturbation experiments in the cat and monkey. L. Goffart

Since a long time, the cerebellum has been assigned a major role in the transformation of sensory signals into motor commands in order to accurately aim an organ like the fovea, the palm of the hand, the nose or the mouth toward the source of sensory signals. But the question of how this sensorimotor transformation is performed by neuronal units and circuits is not solved yet. During my talk, I will summarize results of experiments that were designed to understand how orienting gaze shifts become dysmetric after cerebellar dysfunction.

Long-Lead Burst Neuron Activity during Coordinated Eye-Head Movements. E.G. Freedman

Motor activity in the superior colliculus suggests that the locus of activity specifies the amplitude and direction of impending gaze shifts without regard for the relative contributions of the eyes and/or head that work together to change the direction of the line of sight. Oculomotor activity and activity of excitatory burst neurons appears to be directly related to the actual movements of the eyes on each trial. Between these two populations of neurons Long-Lead Burst Neurons (LLBNs) are anatomically well-placed to contribute to the transformation of gaze commands into eye-specific signals. Recording the activity of LLBNs under conditions in which gaze, eye and head movements can be dissociated will contribute to understanding the mechanisms of this transition.

Coordination of vestibular afferent and corollary discharge (eye position) signals during translation. M. Wei and S.D. Newlands

To maintain visual acuity on the fovea during the translational motion, the geometry of gaze stabilization requires eye movements to be scaled proportionally to the inverse of viewing distance. This stabilization suggests vestibular afferent signals must combine with eye position information to achieve appropriate eye movement during motion. Indeed, previous reports showed that the TVOR is scaled as a function of current eye position. This eye position dependence is not affected even by an upcoming saccade eye movement, which suggests the TVOR modulation might base on the low-level eye position information, such as the proprioceptive information of the ocular plant. However, we found that the central corollary discharge or high-level motor command, rather than the proprioceptive information of the ocular plant, coordinates with the vestibular afferent signal to modulate the gaze stabilization during translational motion.

Integration and adaptation across oculomotor and sensory spatial representations. G.D. Paige, Q. Cui, B. Razavi, and W.E. O’Neill

Vision and audition allow the brain to construct a spatial map of the external world. To maintain space constancy, cross-sensory coherence requires spatial co-calibration as well as accurate accounting for an ever-changing visual frame of reference due to eye movements. We have found that sound localization adaptively adjusts to imposed changes in visual space (optics), but also adapts strongly to sustained changes in eye position alone, suggesting important implications for ocular alignment as well as experimental stalwarts such as prism adaptation

October 5-8 2008, Medford, OR