Modulation of Gaze-Evoked Blinks Depends Primarily on Extraretinal Factors

Gaze-evoked blinks are contractions of the orbicularis oculi (OO)—the lid closing muscle—occurring during rapid movements of the head and eyes and result from a common drive to the gaze and blink motor systems. However, blinks occurring during shifts of gaze are often suppressed when the gaze shift is made to an important visual stimulus, suggesting that the visual system can modulate the occurrence of these blinks. In head-stabilized, human subjects, we tested the hypothesis that the presence of a visual stimulus was sufficient, but not necessary, to modulate OO EMG (OOemg) activity during saccadic eye movements. Rapid, reorienting movements of the eyes (saccades) were made to visual targets that remained illuminated (visually guided trials) or were briefly flashed (memory-guided trials) at different amplitudes along the horizontal meridian. We measured OOemg activity and found that the magnitude and probability of OOemg activity occurrence was reduced when a saccade was made to the memory of the spatial location as well as to the actual visual stimulus. The reduced OOemg activity occurred only when the location of the target was previously cued. OOemg activity occurred reliably with spontaneous saccades that were made to locations with no explicit visual stimulus, generally, back to the fixation location. Thus the modulation of gaze-evoked OOemg activity does not depend on the presence of visual information per se, but rather, results from an extraretinal signal.

Activity Linked to Externally Cued Saccades in Single Units Recorded From Hippocampal, Parahippocampal, and Inferotemporal Areas of Macaques

Sobotka, Stanislaw, Anna Nowicka, and James L. Ringo. Activity linked to externally cued saccades in single units recorded from hippocampal, parahippocampal, and inferotemporal areas of macaques. J. Neurophysiol. 78: 2156–2163, 1997. We studied whether target-directed, externally commanded saccadic eye movements (saccades) induced activity in single units in inferotemporal cortex, the hippocampal formation, and parahippocampal gyrus. The monkeys first were required to fix their gaze on a small cross presented to the left or right of center on the monitor screen. The cross was extinguished, and a random 600–1,000 ms thereafter, a small dot was presented for 200 ms. The dot was located either 10° above, below, right, or left of the position on which the fixation cross had been. The monkey made a saccadic eye movement to this dot (in darkness). The neuronal activity around this goal-directed saccade was analyzed. In addition, control conditions were imposed systematically in which similar dots were presented, but the monkey's task was to withhold the saccade. We recorded 290 units from two monkeys. From this group, 134 met two criteria, they did not show visual response in control trials and they had spike rates >2 Hz. These were analyzed further; 53% (71/134) showed modulation related to the target directed saccade, and 29% (39/134) showed saccadic modulation during spontaneous eye movements. These two groups were correlated only weakly. Of the units with significant saccadic modulation, 17% (12/71) showed significant directional selectivity, and 13% (9/71) showed significant position selectivity ( P < 0.01). At a lower criterion ( P < 0.05), almost one-half (33/71) showed one or the other spatial selectivity. Primates use saccades to acquire visual information. The appearance of strong saccadic modulation in brain structures previously characterized as mnemonic suggests the possibility that the mnemonic circuitry uses an extraretinal signal linked to saccades to control visual memory processes, e.g., synchronizing mnemonic processes to the pulsatile visual data inflow.

A Computational Model of the Eye Movement Effects on Motion Perception

Accurate speed and direction matches can be made between a moving stimulus viewed with a stationary eye and a moving stimulus viewed with an eye moving in the opposite direction to the stimulus. However, when the eye moves in the same direction as the distal stimulus, at a slower speed, subjects match the retinal-image motions of the stimuli rather than their distal motions (Heidenreich and Turano, 1995 Investigative Ophthalmology and Visual Science36 1675). Furthermore, it is only under this latter condition (and when the eye is stationary) that subjects can precisely discriminate distal stimulus speeds (Turano and Heidenreich Vision Research in press). We present a computational model that can account for the results of all three findings. The model assumes that the extraretinal signal mirrors the eye movement. Motion information from the retinal and extraretinal sources is combined in a subtractive manner when the two signals have opposite sign. When the two signals have the same sign, they do not combine, and motion judgments are based solely on information from the retinal source.

Visual responses of pulvinar and collicular neurons during eye movements of awake, trained macaques

1. We recorded from single neurons in awake, trained rhesus monkeys in a lighted environment and compared responses to stimulus movement during periods of fixation with those to motion caused by saccadic or pursuit eye movements. Neurons in the inferior pulvinar (PI), lateral pulvinar (PL), and superior colliculus were tested. 2. Cells in PI and PL respond to stimulus movement over a wide range of speeds. Some of these cells do not respond to comparable stimulus motion, or discharge only weakly, when it is generated by saccadic or pursuit eye movements. Other neurons respond equivalently to both types of motion. Cells in the superficial layers of the superior colliculus have similar properties to those in PI and PL. 3. When tested in the dark to reduce visual stimulation from the background, cells in PI and PL still do not respond to motion generated by eye movements. Some of these cells have a suppression of activity after saccadic eye movements made in total darkness. These data suggest that an extraretinal signal suppresses responses to visual stimuli during eye movements. 4. The suppression of responses to stimuli during eye movements is not an absolute effect. Images brighter than 2.0 log units above background illumination evoke responses from cells in PI and PL. The suppression appears stronger in the superior colliculus than in PI and PL. 5. These experiments demonstrate that many cells in PI and PL have a suppression of their responses to stimuli that cross their receptive fields during eye movements. These cells are probably suppressed by an extraretinal signal. Comparable effects are present in the superficial layers of the superior colliculus. These properties in PI and PL may reflect the function of the ascending tectopulvinar system.

Retinal and Extraretinal Information in Movement Perception: How to Invert the Filehne Illusion

During a pursuit eye movement made in darkness across a small stationary stimulus, the stimulus is perceived as moving in the opposite direction to the eyes. This so-called Filehne illusion is usually explained by assuming that during pursuit eye movements the extraretinal signal (which informs the visual system about eye velocity so that retinal image motion can be interpreted) falls short. A study is reported in which the concept of an extraretinal signal is replaced by the concept of a reference signal, which serves to inform the visual system about the velocity of the retinae in space. Reference signals are evoked in response to eye movements, but also in response to any stimulation that may yield a sensation of self-motion, because during self-motion the retinae also move in space. Optokinetic stimulation should therefore affect reference signal size. To test this prediction the Filehne illusion was investigated with stimuli of different optokinetic potentials. As predicted, with briefly presented stimuli (no optokinetic potential) the usual illusion always occurred. With longer stimulus presentation times the magnitude of the illusion was reduced when the spatial frequency of the stimulus was reduced (increased optokinetic potential). At very low spatial frequencies (strongest optokinetic potential) the illusion was inverted. The significance of the conclusion, that reference signal size increases with increasing optokinetic stimulus potential, is discussed. It appears to explain many visual illusions, such as the movement aftereffect and center–surround induced motion, and it may bridge the gap between direct Gibsonian and indirect inferential theories of motion perception.