From following edges to pursuing objects

Primates can generate accurate, smooth eye-movement responses to moving target objects of arbitrary shape and size, even in the presence of complex backgrounds and/or the extraneous motion of non-target objects. Most previous studies of pursuit have simply used a spot moving over a featureless background as the target and have thus neglected critical issues associated with the general problem of recovering object motion. Visual psychophysicists and theoreticians have shown that, for arbitrary objects with multiple features at multiple orientations, object-motion estimation for perception is a complex, multi-staged, time-consuming process. To examine the temporal evolution of the motion signal driving pursuit, we recorded the tracking eye movements of human observers to moving line-figure diamonds. We found that pursuit is initially biased in the direction of the vector average of the motions of the diamond's line segments and gradually converges to the true object-motion direction with a time constant of approximately 90 ms. Furthermore, transient blanking of the target during steady-state pursuit induces a decrease in tracking speed, which, unlike pursuit initiation, is subsequently corrected without an initial direction bias. These results are inconsistent with current models in which pursuit is driven by retinal-slip error correction. They demonstrate that pursuit models must be revised to include a more complete visual afferent pathway, which computes, and to some extent latches on to, an accurate estimate of object direction over the first hundred milliseconds or so of motion.     

A neuronal correlate of spatial stability during periods of self-induced visual motion

Summary Motion of background visual images across the retina during slow tracking eye movements is usually not consciously perceived so long as the retinal image motion results entirely from the voluntary slow eye movement (otherwise the surround would appear to move during pursuit eye movements). To address the question of where in the brain such filtering might occur, the responses of cells in 3 visuo-cortical areas of macaque monkeys were compared when retinal image motion of background images was caused by object motion as opposed to a pursuit eye movement. While almost all cells in areas V4 and MT responded indiscriminately to retinal image motion arising from any source, most of those recorded in the dorsal zone of area MST (MSTd), as well as a smaller proportion in lateral MST (MST1), responded preferentially to externally-induced motion and only weakly or not at all to self-induced visual motion. Such cells preserve visuo-spatial stability during low-velocity voluntary eye movements and could contribute to the process of providing consistent spatial orientation regardless of whether the eyes are moving or stationary.     

Directional tuning of motion-sensitive cells in the anterior superior temporal polysensory area of the macaque

An investigation was made into the directional sensitivity of cells in the macaque anterior superior temporal polysensory region (STPa) to the motion of objects. The cells studied were sensitive to the presence of motion but showed little or no selectivity for the form of the stimulus. Directional tuning was not continuously distributed about all possible directions. The majority of cells were most responsive to motion in a direction within 15° of one of the three cartesian axes (up/down, left/right, towards/away). Tuning to direction varied in sharpness. For most (34/37) cells the angular change in direction required to reduce response to half maximal was between 45 and 70° (for 3/37 cells it was > 90°). The estimates of the directionality (median I _d = 0.97) of STPa cells was similar to that reported for posterior motion processing areas (the middle temporal area, MT, and the medial superior temporal area, MST). The tuning for direction (sharpness, distribution and discrimination) of the motion-sensitive STPa cells were found to be similar to the tuning for perspective view of STPa cells selective for static form of the head and body. On average the STPa responses showed a 100- to 300-ms transient burst of activity followed by a tonic discharge maintained at approximately 20% of the peak firing rate for the duration of stimulation. The responses of motion-sensitive STPa cells occurred at an earlier latency (mean 91 ms) than responses of cells selective for static form (mean 119 ms), but the time course of responses of the two classes of cell were similar in many other respects. The early response latency and directional selectivity indicate that motion sensitivity in STPa cells derives from the dorsal visual pathway via MT/MST. The similarity of tuning for direction and perspective view within STPa may facilitate the integration of motion and form processing within this high-level brain area.     

Eye movements cannot explain vibration-induced visual motion and motion aftereffect

Eye movements are thought to account for a number of visual motion illusions involving stationary objects presented against a featureless background or apparent motion of the whole visual field. We tested two different versions of the eye movement account: (a) the retinal slip explanation and (b) the nystagmus-suppression explanation, in particular their ability to account for visual motion experienced during vibration of the neck muscles, and for the visual motion aftereffect following vibration. We vibrated the neck (ventral sternocleidomastoid muscles, bilaterally, or right dorsal muscles) and measured eye movements in conjunction with perceived illusory displacement of an LED presented in complete darkness (N=10). To test the retinal-slip explanation, we compared the direction of slow eye movements to the direction of illusory motion of the visual target. To test the suppression explanation, we estimated the direction of suppressed slow-phase eye movements and compared it to the direction of illusory motion. Two main findings show that neither actual nor suppressed eye movements cause the illusory motion and motion aftereffect. Firstly, eye movements do not reverse direction when the illusory motion reverses after vibration stops. Secondly, there are large individual differences with regards to the direction of eye movements in observers who all experience a similar visual illusion. We conclude that, rather than eye movements, a more global spatial constancy mechanism that takes into account head movement is responsible for the illusion. The results also argue against the notion of a single central signal that determines both perceptual experience and oculomotor behaviour.     

Object motion computation for the initiation of smooth pursuit eye movements in humans

Pursuing an object with smooth eye movements requires an accurate estimate of its two-dimensional (2D) trajectory. This 2D motion computation requires that different local motion measurements are extracted and combined to recover the global object-motion direction and speed. Several combination rules have been proposed such as vector averaging (VA), intersection of constraints (IOC), or 2D feature tracking (2DFT). To examine this computation, we investigated the time course of smooth pursuit eye movements driven by simple objects of different shapes. For type II diamond (where the direction of true object motion is dramatically different from the vector average of the 1-dimensional edge motions, i.e., VA not equal IOC = 2DFT), the ocular tracking is initiated in the vector average direction. Over a period of less than 300 ms, the eye-tracking direction converges on the true object motion. The reduction of the tracking error starts before the closing of the oculomotor loop. For type I diamonds (where the direction of true object motion is identical to the vector average direction, i.e., VA = IOC = 2DFT), there is no such bias. We quantified this effect by calculating the direction error between responses to types I and II and measuring its maximum value and time constant. At low contrast and high speeds, the initial bias in tracking direction is larger and takes longer to converge onto the actual object-motion direction. This effect is attenuated with the introduction of more 2D information to the extent that it was totally obliterated with a texture-filled type II diamond. These results suggest a flexible 2D computation for motion integration, which combines all available one-dimensional (edge) and 2D (feature) motion information to refine the estimate of object-motion direction over time.     

Direction and speed tuning to visual motion in cortical areas MT and MSTd during smooth pursuit eye movements

When tracking a moving target in the natural world with pursuit eye movement, our visual system must compensate for the self-induced retinal slip of the visual features in the background to enable us to perceive their actual motion. We previously reported that the speed of the background stimulus in space is represented by dorsal medial superior temporal (MSTd) neurons in the monkey cortex, which compensate for retinal image motion resulting from eye movements when the direction of the pursuit and background motion are parallel to the preferred direction of each neuron. To further characterize the compensation observed in the MSTd responses to the background motion, we recorded single unit activities in cortical areas middle temporal (MT) and MSTd, and we selected neurons responsive to a large-field visual stimulus. We studied their responses to the large-field stimulus in the background while monkeys pursued a moving target and while fixated a stationary target. We investigated whether compensation for retinal image motion of the background depended on the speed of pursuit. We also asked whether the directional selectivity of each neuron in relation to the external world remained the same even during pursuit and whether compensation for retinal image motion occurred irrespective of the direction of the pursuit. We found that the majority of the MSTd neurons responded to the visual motion in space by compensating for the image motion on the retina resulting from the pursuit regardless of pursuit speed and direction, whereas most of the MT neurons responded in relation to the genuine retinal image motion.     

Human ocular responses to translation of the observer and of the scene: dependence on viewing distance

Recent experiments on monkeys have indicated that the eye movements induced by brief translation of either the observer or the visual scene are a linear function of the inverse of the viewing distance. For the movements of the observer, the room was dark and responses were attributed to a translational vestibulo-ocular reflex (TVOR) that senses the motion through the otolith organs; for the movements of the scene, which elicit ocular following, the scene was projected and adjusted in size and speed so that the retinal stimulation was the same at all distances. The shared dependence on viewing distance was consistent with the hypothesis that the TVOR and ocular following are synergistic and share central pathways. The present experiments looked for such dependencies on viewing distance in human subjects. When briefly accelerated along the interaural axis in the dark, human subjects generated compensatory eye movements that were also a linear function of the inverse of the viewing distance to a previously fixated target. These responses, which were attributed to the TVOR, were somewhat weaker than those previously recorded from monkeys using similar methods. When human subjects faced a tangent screen onto which patterned images were projected, brief motion of those images evoked ocular following responses that showed statistically significant dependence on viewing distance only with low-speed stimuli (10°/s). This dependence was at best weak and in the reverse direction of that seen with the TVOR, i.e., responses increased as viewing distance increased. We suggest that in generating an internal estimate of viewing distance subjects may have used a confounding cue in the ocular-following paradigm the size of the projected scene -which was varied directly with the viewing distance in these experiments (in order to preserve the size of the retinal image). When movements of the subject were randomly interleaved with the movements of the scene to encourage the expectation of ego-motion -the dependence of ocular following on viewing distance altered significantly: with higher speed stimuli (40°/s) many responses (63%) now increased significantly as viewing distance decreased, though less vigorously than the TVOR. We suggest that the expectation of motion results in the subject placing greater weight on cues such as vergence and accommodation that provide veridical distance information in our experimental situation: cue selection is context specific.     

Human ocular responses to translation of the observer and of the scene: dependence on viewing distance

Recent experiments on monkeys have indithat-—the eye movements induced by brief translation of either the observer or the visual scene are a linear function of the inverse of the viewing distance. For the movements of the observer, the room was dark and responses were attributed to a translational vestibulo-ocular reflex (TVOR) that senses the motion through the otolith organs; for the movements of the scene, which elicit ocular following, the scene was projected and adjusted in size and speed so that the retinal stimulation was the same at all distances. The shared dependence on viewing distance was consistent with the hypothesis that the TVOR and ocular following are synergistic and share central pathways. The present experiments looked for such dependencies on viewing distance in human subjects. When briefly accelerated along the interaural axis in the dark, human subjects generated compensatory eye movements that were also a linear function of the inverse of the viewing distance to a previously fixated target. These responses, which were attributed to the TVOR, were somewhat weaker than those previously recorded from monkeys using similar methods. When human subjects faced a tangent screen onto which patterned images were projected, brief motion of those images evoked ocular following responses that showed statistically significant dependence on viewing distance only with low-speed stimuli (10°/s). This dependence was at best weak and in the reverse direction of that seen with the TVOR, i.e., responses increased as viewing distance increased. We suggest that in generating an internal estimate of viewing distance subjects may have used a confounding cue in the ocular-following paradigmthe size of the projected scene - which was varied directly with the viewing distance in these experiments (in order to preserve the size of the retinal image). When movements of the subject were randomly interleaved with the movements of the scene - to encourage the expectation of ego-motion - the dependence of ocular following on viewing distance altered significantly: with higher speed stimuli (40°/s) many responses (63%) now increased significantly as viewing distance decreased, though less vigorously than the TVOR. We suggest that the expectation of motion results in the subject placing greater weight on cues such as vergence and accommodation that provide veridical distance information in our experimental situation: cue selection is context specific.     

Visual motion due to eye movements helps guide the hand

Movement of the body, head, or eyes with respect to the world creates one of the most common yet complex situations in which the visuomotor system must localize objects. In this situation, vestibular, proprioceptive, and extra-retinal information contribute to accurate visuomotor control. The utility of retinal motion information, on the other hand, is questionable, since a single pattern of retinal motion can be produced by any number of head or eye movements. Here we investigated whether retinal motion during a smooth pursuit eye movement contributes to visuomotor control. When subjects pursued a moving object with their eyes and reached to the remembered location of a separate stationary target, the presence of a moving background significantly altered the endpoints of their reaching movements. A background that moved with the pursuit, creating a retinally stationary image (no retinal slip), caused the endpoints of the reaching movements to deviate in the direction of pursuit, overshooting the target. A physically stationary background pattern, however, producing retinal image motion opposite to the direction of pursuit, caused reaching movements to become more accurate. The results indicate that background retinal motion is used by the visuomotor system in the control of visually guided action.     

Relationship between extraretinal component of firing rate and eye speed in area MST of macaque monkeys

We have isolated extraretinal and retinal components of firing during smooth pursuit eye movements in the medial-superior-temporal area (MST) in the extrastriate visual cortex. Awake macaque monkeys tracked spots in total darkness to eliminate image motion inputs from the background. For 300 ms during sustained tracking at different speeds, the target was stabilized on the moving eye, practically eliminating image motion inputs from the tracking target. The extraretinal component of firing rate during image stabilization was direction selective and related to eye speed but sometimes showed a different preferred speed from the retinal component of the same neuron's responses. The highly variable firing rate of individual MST neurons allowed an ideal observer to predict target speed correctly on 25% of trials. Pooling the data from 71 MST neurons improved the correct response rate to 50%. Behavioral experiments imposed brief perturbations of target velocity to assess the gain of visual-motor transmission for pursuit. The average response to perturbations increased as a function of target speed. However, the size of the responses to individual perturbations allowed an ideal observer to predict target speed correctly on only 35% of the trials. The imprecision of MST responses argues that the output of MST may be a poor candidate to drive eye velocity and so may instead regulate another component of pursuit. The good agreement between the eye velocity precision of the behavioral responses to perturbations of target motion and the firing of MST neurons raises regulation of the visual-motor gain of pursuit as one candidate component.     

Relation of cortical areas MT and MST to pursuit eye movements. III. Interaction with full-field visual stimulation

1. Pursuit eye movements are usually made against a visual background that is moved across the retina by the pursuit movement. We have investigated the effect of this visual stimulation on the response of pursuit cells that lie within the superior temporal sulcus (STS) of the monkey. 2. We assigned these pursuit cells to one of two groups depending on the nature of their preferred visual stimulus. One group of cells, comprising all cells located in the dorsal-medial region of the medial superior temporal area (MSTd) and some cells in lateral-anterior MST (MST1), responded to the motion of a large patterned field but showed little or no response to small spots or slits. The other group, consisting of all foveal middle temporal area (MTf) cells and many MST1 cells, responded preferentially to small spot motion or equally well to small spot motion or large field. 3. For many pursuit cells that preferred large-field stimuli, the visual response showed a reversal of the preferred direction of motion as the size of the stimulus field increased. The reversal usually occurred as the size of the moving random-dot field used as a stimulus increased in size from 20 x 20 degrees to 30 x 30 degrees for motion at approximately 10 degrees/s. The size of the filed stimulus leading to reversal of preferred direction depended on the speed of stimulus motion. Higher speeds of motion required larger stimulus fields to produce a reversal of preferred direction. This reversal (of preferred direction) did not reflect a center-surround organization of the receptive field but seemed to reflect the spatial summation properties of these cells. 4. For three-quarters of the cells that preferred large-field stimulation, the preferred direction of motion for the large field was opposite to the preferred direction of the pursuit response. The remaining cells showed either the same preferred directions for large-field visual stimulation and the pursuit response or had bidirectional visual responses. If we consider only the cells that show a reversal of preferred direction for large- and small-field stimuli, the preferred direction for the large field was always the opposite to that of pursuit, and the preferred direction for the small field was always the same. 5. During pursuit against a lighted background, the cells that showed opposite preferred directions for large-field stimulation and pursuit had synergistic responses--a facilitation of the pursuit response over the response during pursuit in the dark. Slow pursuit speeds (less than 20 degrees/s) produced the greatest facilitation.(ABSTRACT TRUNCATED AT 400 WORDS)     

The distinction between eye and object motion is reflected by the motion-onset visual evoked potential

Humans are able to distinguish eye movement-induced retinal image motion and physical object motion during smooth pursuit eye movements. We investigated the neurophysiological basis of this ability by comparing motion-onset visual evoked potentials (VEPs) to onset of: (1) physical object motion during fixation, (2) eye movement-induced retinal image motion, and (3) physical object motion during eye movements. Electro-oculographic (EOG) artifacts were removed and the influence of eye-movement quality was evaluated. Retinal image shift was of similar magnitude in all conditions (9 degrees /s) and elicited typical motion-onset VEPs, with N2 at occipital and P2 at central derivations. During smooth pursuit, physical object motion induced N2 and P2 of higher latencies than during fixation. In the absence of physical object motion, i.e., for exclusively eye movement-induced retinal image motion, the N2 amplitude was reduced. This is taken as evidence that the activity of detectors of physical object motion is reflected by a part of the N2 component. N2 also reflects eye movement-induced retinal image motion. It is concluded that headcentric motion detection and the detection of eye movement-induced retinal image motion is mediated by brain mechanisms with similar latencies and, within the resolution limits of VEPs, at similar locations.     

Electrophysiological evidence for visual-vestibular interaction in man

The aim of the experiments reported here was to confirm electrophysiologically the results of psychophysical experiments, which demonstrated that thresholds for object-motion detection are significantly raised during both concurrent active or passive sinusoidal head oscillations and during visually induced self-motion perception (circularvection, CV). This intersensory inhibition could now be demonstrated electrophysiologically by recording visual motion evoked potentials both during concurrent sinusoidal head oscillations and during visually induced apparent self-motion of the objectively stationary subject. Recordings of visual contrast reversal evoked potentials failed to reveal such an interaction. Perceptual phenomena with multisensory stimulation are well described in the literature. Berthoz et al. demonstrated the dominant influence of the visual channel on vestibular thresholds such that the detection of a suprathreshold vestibular stimulation was clearly impaired by a simultaneously moving visual pattern inducing linearvection and vice versa. Comparable results are reported for circularvection. Evidence for inhibitory interaction between object-motion and simultaneous self-motion perception also exists. Electrophysiological data on intersensory interaction in humans have only been reported between electrical stimulation of a limb and its concurrent movement by means of scalp-recorded somatosensory-evoked potentials (SSEPs) (e.g. refs. 3, 5). Electrophysiological evidence for the interaction of visual object-motion and vestibular self-motion perception in humans has never been reported in the literature thus far, though Hood and Kayan demonstrated that retinal image motion makes a contribution to the vestibularly evoked bioelectric response.     

Smooth-pursuit eye movements elicited by first-order and second-order motion

 The perception of the displacement of luminance-defined contours (i.e., first-order motion) is an important and well-examined function of the visual system. It can be explained, for example, by the operation of elementary motion detectors (EMDs), which cross-correlate the spatiotemporal luminance distribution. More recent studies using second-order motion stimuli, i.e., shifts of the distribution of features such as contrast, texture, flicker, or motion, extended classic concepts of motion perception by including nonlinear or hierarchical processing in the EMD. Smooth-pursuit eye movements can be used as a direct behavioral probe for motion processing. The ability of the visual system to extract motion signals from the spatiotemporal changes of the retinal image can be addressed by analyzing the elicited eye movements. We measured the eye movement response to moving objects defined by two different types of first-order motion and two different types of second-order motion. Our results clearly showed that the direction of smooth-pursuit eye movements was always determined by the direction of object motion. In particular, in the case of second-order motion stimuli, smooth-pursuit did not follow the retinal image motion. The latency of the initial saccades during pursuit of second-order stimuli was slightly but significantly increased, compared with the latency of saccades elicited by first-order motion. The processing of second-order motion in the peripheral visual field was less exact than the processing of first-order motion in the peripheral field. Steady state smooth-pursuit eye speed did not reflect the velocity of second-order motion as precisely as that of first-order motion, and the resulting retinal error was compensated by saccades. Interestingly, for slow second-order stimuli we observed that the eye could move faster than the target, leading to small, corrective saccades in the opposite direction to the ongoing smooth-pursuit eye movement. We conclude from our results that both visual perception and the control of smooth-pursuit eye movements have access to processing mechanisms extracting first- and second-order motion. Received: 26 August 1996 / Accepted: 8 November 1996     

Visually mediated eye movements regulate the capture of optic flow in self-motion perception

Eye movements help capture optic-flow information necessary to perceive visually our self motion. Visual and vestibular systems control compensatory eye movements that serve to stabilize the retinal images we capture. We examined the role that these eye movements may play in generating visual illusions of self motion (or vection). Observers viewed radially expanding optic-flow displays while performing lateral translational head oscillations at 1 Hz. Simulated viewpoint changes in these displays were synchronized with head movements, either in an ipsilateral (minimal sensory conflict) or a contralateral (high sensory conflict) direction. In control conditions, the observer viewed purely radial displays. Vection-onset latency and overall vection strength ratings were recorded, as well as horizontal eye movements. Vection onsets and strength ratings were significantly greater when the observer’s head movements were incorporated into the visual displays. However, vection strength ratings were very similar for both ipsilateral and contralateral active display oscillation. Surprisingly, the non-ecological contralateral viewpoint oscillation actually induced vection earlier, despite the relatively small eye-in-head rotations coordinating gaze in these conditions. Our results support the view that compensatory eye movements are controlled through cooperative visual and vestibular interactions, and show that linear vection is highly robust against large sensory conflicts.     

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.     

Retrograde transneuronal transport of wheat-germ agglutinin to the retina from visual cortex in the cat

Summary The stability of visual perception despite eye movements suggests the existence, in the visual system, of neural elements able to recognize whether a movement of an image occurring in a particular part of the retina is the consequence of an actual movement that occurred in the visual field, or self-induced by an ocular movement while the object was still in the field of view. Recordings from single neurons in area V3A of awake macaque monkeys were made to check the existence of such a type of neurons (called real-motion cells; see Galletti et al. 1984, 1988) in this prestriate area of the visual cortex. A total of 119 neurons were recorded from area V3A. They were highly sensitive to the orientation of the visual stimuli, being on average more sensitive than V1 and V2 neurons. Almost all of them were sensitive to a large range of velocities of stimulus movement and about one half to the direction of it. In order to assess whether they gave different responses to the movement of a stimulus and to that of its retinal image alone (self-induced by an eye movement while the stimulus was still), a comparison was made between neuronal responses obtained when a moving stimulus swept a stationary receptive field (during steady fixation) and when a moving receptive field swept a stationary stimulus (during tracking eye movement). The receptive field stimulation at retinal level was physically the same in both cases, but only in the first was there actual movement of the visual stimulus. Control trials, where the monkeys performed tracking eye movements without any intentional receptive field stimulation, were also carried out. For a number of neurons, the test was repeated in darkness and against a textured visual background. Eighty-seven neurons were fully studied to assess whether they were real-motion cells. About 48% of them (42/87) showed significant differences between responses to stimulus versus eye movement. The great majority of these cells (36/42) were real-motion cells, in that they showed a weaker response to visual stimulation during tracking than to the actual stimulus movement during steady fixation. On average, the reduction in visual response during eye movement was 64.0 ± 15.7% (SD). Data obtained with a uniform visual background, together with those obtained in darkness and with textured background, indicate that real-motion cells receive an eye-motion input, either retinal or extraretinal in nature, probably acting presynaptically on the cell's visual input. In some cases, both retinal and extraretinal eye-motion inputs converge on the same real-motion cell. No correlation was observed between the real-motion behaviour and the sensitivity to either orientation or direction of movement of the visual stimulus used to activate the receptive field, nor with the retinotopic location of the receptive field. We suggest that the visual system uses real-motion cells in order to distinguish real from self-induced movements of retinal images, hence to recognize the actual movement in the visual field. Based on psychophysical data, the hypothesis has been advanced of an internal representation of the field of view, stable despite eye movement (cf. MacKay 1973). The real-motion cells may be neural elements of this network and we suggest that the visual system uses the output of this network to properly interpret the large number of sensory changes resulting from exploratory eye movements in a stable visual world.     

Visual signals in the dorsolateral pontine nucleus of the alert monkey: Their relationship to smooth-pursuit eye movements

Summary The visual properties of 77 dorsolateral pontine nucleus (DLPN) cells were studied in two alert monkeys. In 41 cells, presentation of a moving random dot background pattern, while the monkeys fixated a stationary spot, elicited modulations in discharge rate that were related either to (i) the velocity of background motion in a specific direction or to (ii) only the direction of background movement. Thirty-six DLPN cells exhibited responses to small, 0.6–1.7 deg, visual stimuli. Nine such cells exhibited non-direction selective receptive fields that were eccentric from the fovea. During fixation of a stationary bluish spot, the visual responses of 27 DLPN cells to movement of a small, white test spot were characterized by two components: (1) as the test spot crossed the fovea in a specific direction, transient velocity-related increases in discharge rate occurred and (2) a maintained, smaller increase in activity was observed for the duration of test spot movement in the preferred direction. This DLPN activity associated with small visual stimuli was also observed during smooth-pursuit eye movements when, due to imperfect tracking, retinal image motion of the target produced slip in the same direction. These preliminary results suggest that the DLPN could supply the smooth-pursuit system with signals concerning the direction and velocity of target image motion on the retina.This study was supported by NSF Grant BNS-8107111, NIH Grant R01 EY04552-01, and the Smith-Kettlewell Eye Research Foundation Dedication. This paper is dedicated to Dr. Kitsuya Iwama, Emeritus Professor of Osaka University Medical School, on his retirement. The first author is grateful for the inspiration and guidance that Dr. Iwama provided during the early part of the author's education in neurophysiology.     

The role of the posterior vermis of monkey cerebellum in smooth-pursuit eye movement control. II. Target velocity-related Purkinje cell activity

1. Purkinje cell activity was recorded from lobules VI and VII of the cerebellar vermis during the performance of visuooculomotor tasks designed to dissociate the signals related to head, smooth-pursuit eye, and retinal image movements. Task-related modulations in the simple spike discharge rates of 157 cells were observed in three alert monkeys. 2. Of 65 Purkinje cells that were completely tested for all three signals, all exhibited smooth-pursuit eye movement-related activity. An additional vestibular or visual response was observed in 17 and 11% of the cells, respectively. Eye, head, and retinal image velocity signals were all recorded in the same unit in 52% of the Purkinje cells. The responses of 5% of the fully tested cells were associated with changes in the direction of eye, head, and retinal image movement. 3. The observed sensorioculomotor responses were direction selective in 98% of the Purkinje cells. For the Purkinje cells that were fully tested, 60% of the cells exhibited peak discharge rates for ipsilateral and 40% for contralateral eye velocity. Of these Purkinje cells, 45% exhibited eye, head, and retinal image velocity signals with equivalent direction preferences. 4. Of 42 Purkinje cells tested, 88% demonstrated some kinds of interactive responses during combined eye and sensory stimulation. The interaction of eye and head velocity signals has been discussed in a companion paper (38). The modulation in discharge rate observed during tracking in the presence of a random dot background pattern could be predicted from the dissociated responses to smooth pursuit in the dark and to movements of the background pattern during suppression of eye movements. 5. The sensitivity to smooth-pursuit eye velocity averaged 1.4 times the sensitivity to head velocity. In 80% of the Purkinje cells, however, the sensitivity to eye velocity exceeded the sensitivity to head velocity by an average of only 10%. The sensitivity to smooth-pursuit eye velocity averaged 1.6 times the sensitivity to retinal image velocity. 6. An increase in Purkinje cell discharge rate was observed during the open-loop period of the initiation of smooth-pursuit eye movements. This open-loop response was consistent with the presence of a visual signal during ocular pursuit, since these cells were also shown to be responsive to a dissociated retinal image velocity signal. Furthermore, the magnitude of the open-loop response indicated an enhancement of the sensitivity to retinal image velocity when visual information became behaviorally significant.(ABSTRACT TRUNCATED AT 400 WORDS)     

Are the Eye Movements of Dreaming Sleep Related to the Visual Images of the Dreams?

As a result of recording eye movements during Stage REM sleep by AC electrooculography (EOG) previous investigators concluded that each eye movement is the response to the visual action in each dream. When we repeated the study using DC EOG it was discovered that only a minority of eye movements during Stage REM are in the direction of the visual action in the dream. If only single, large amplitude, prominent eye movements are considered then most such movements are related to colorful, compelling visual action occurring as a prominent single visual action against a quiet background. The AC recording method used in past studies emphasizes these isolated movements; perhaps this explains the disparity in results. At any rate, most eye movements during REM sleep are unrelated to the action in the dream. When these eye movements were analyzed in regard to the direction of movements, sequential order of movements, and randomness in time, we found that similar patterns of oculomotor output were found in all subjects. Thus, the nervous system executes a patterned output of oculomotor activity during dreaming sleep which is fairly consistent in all subjects. At times, however, a link is established between the visual and oculomotor systems and the eyes respond to visual action.