Characterization of pretectal-nuclear-complex afferents to the pulvinar in the cat

We investigated anatomical and physiological properties of the projection from the pretectal nuclear complex (PNC) to the ipsilateral lateral posterior–pulvinar complex in the cat. After Phaseolus vulgaris leucoagglutinin injections into the PNC, the majority (70%) of anterogradely labeled terminals was localized in the pulvinar proper, the remaining 30% were scattered in the lateral and medial portions of the LP. No PNC neuron retrogradely labeled from the pulvinar was found to also express glutamic acid decarboxylase (GAD) mRNA, although a large number of neurons carrying the GAD label were found in close vicinity. In contrast, 69% of retrogradely labeled PNC cells also displayed glutamate-like immunoreactivity. Twenty-six out of 96 (27%) visually responsive pulvinar neurons were orthodromically activated by electrical stimulation of the ipsilateral PNC at latencies between 1 and 10 ms (median 1.9 ms). All orthodromically activated neurons responded well to the onset and offset of large visual stimuli and to sudden stimulus shifts. Whenever a saccadic eye movement was executed, these neurons were also activated, except during saccades in darkness. The comparison of saccade-evoked response with responses to visual stimuli that elicit similar retinal image shifts revealed that pretectorecipient pulvinar neurons also seem to receive a saccade-related non-visual input. All response properties correspond to those of a specific class of pulvinar neurons that have been termed "SV" neurons because they respond to visual stimulation as well as during saccades. They also closely resemble response properties of PNC neurons that project to the ipsilateral pulvinar. The results support the proposal that PNC cells not only directly activate their postsynaptic target neurons in the pulvinar, but that they also provide a visual input to these neurons that greatly contributes to their response characteristics. Electronic Publication     

Response properties of relay cells in the A-laminae of the cat's dorsal lateral geniculate nucleus after saccades

Responses of relay cells in the A-laminae of the dorsal lateral geniculate nucleus (LGNd) during spontaneous saccades and saccade-like visual stimulation were extracellularly recorded in awake cats. Ninety-six out of 137 cells recorded (42 X and 54 Y cells) were responsive during spontaneous saccadic eye movements. All Y cells and 67% of the X cells responded with burst activity, i.e. with either one or two activity peaks during and after saccades. Thirty-three percent of the X cells were inhibited during saccades. Excitatory peaks occurred at mean latencies of 33 ms and 31 ms for X and Y cells, respectively. Comparable burst responses were obtained when retinal image shifts similar to those during saccades were induced by external saccade-like stimulus movements. However, the latencies of excitatory peak activity were significantly longer to external stimuli than to the onsets of saccades. This indicates the existence of an eye movement-related input which activates LGNd relay cells in addition to the visual input. We propose that the pretectogeniculate projection may contribute to the responses of LGNd relay cells following saccadic eye movements via a disinhibitory input and that this input could be involved in intra- and postsaccadic modulations of the transfer of visual signals to visual cortex.     

Rapid processing of retinal slip during saccades in macaque area MT

The primate middle temporal area (MT) is involved in the analysis and perception of visual motion, which is generated actively by eye and body movements and passively when objects move. We studied the responses of single cells in area MT of awake macaques, comparing the direction tuning and latencies of responses evoked by wide-field texture motion during fixation (passive viewing) and during rewarded, target-directed saccades and non-rewarded, spontaneous saccades over the same stationary texture (active viewing). We found that MT neurons have similar motion sensitivity and direction-selectivity for retinal slip associated with active and passive motion. No cells showed reversals in direction tuning between the active and passive viewing conditions. However, mean latencies were significantly different for saccade-evoked responses (30 ms) and stimulus-evoked responses (67 ms). Our results demonstrate that neurons in area MT retain their direction-selectivity and display reduced processing times during saccades. This rapid, accurate processing of peri-saccadic motion may facilitate post-saccadic ocular following reflexes or corrective saccades.     

Activity of rostral superior colliculus neurons during passive and active viewing of motion

The superior colliculus (SC) has long been known to be important for the control of saccades, and recent findings indicate that the rostral SC (rSC) plays some role in pursuit as well. The recent finding that the prelude activity of some SC neurons exhibits directional selectivity suggests that the rSC might process visual motion signals relevant for the control of pursuit. We have now tested the activity of buildup neurons in the rSC during the passive viewing of motion stimuli placed within their response field and also during the previewing of visual motion stimuli that were subsequently tracked with pursuit eye movements. We found that rSC buildup neurons typically responded well to motion stimuli, but that they exhibited essentially no selectivity for the direction or speed of visual motion, and that they also responded well to stationary flickering dots. However, during the previewing of visual motion prior to the onset of pursuit, many neurons did exhibit a buildup of activity similar to that exhibited before saccades. These results are inconsistent with the notion that the rSC mediates visual motion signals used to drive pursuit, but instead support the idea that visual motion signals can be used by rSC neurons as part of a mechanism for selecting targets for pursuit and saccades.     

Non-visually evoked activity of isthmo-optic neurons in awake,head-unrestrained quail

Changes in the internal state of the brain may modulate retinal function. In birds, most neurons in the isthmo-optic (IO) nucleus project their axons topographically into the contralateral retina, and activity in IO neurons enhances visual responses of retinal ganglion cells in the target retinal region. To elucidate the significance of this pathway, we recorded spikes of IO neurons in four awake Japanese quail using an implanted electrode assembly while recording unrestrained head movements. The IO neurons fired passively in response to visual stimuli in receptive fields and non-visually without visual stimuli or eye–head movements. Non-visually evoked activity was observed in the middle of eye–head fixation, as well as at about 200 ms before the onset of head saccades. Intensity of activity before onset of head saccades depended on the direction of motion of subsequent head saccades. Local retinal output may be enhanced by centrifugal signals before gaze shifts.     

Role of arcuate frontal cortex of monkeys in smooth pursuit eye movements. I. Basic response properties to retinal image motion and position

Anatomical and physiological studies have shown that the "frontal pursuit area" (FPA) in the arcuate cortex of monkeys is involved in the control of smooth pursuit eye movements. To further analyze the signals carried by the FPA, we examined the activity of pursuit-related neurons recorded from a discrete region near the arcuate spur during a variety of oculomotor tasks. Pursuit neurons showed direction tuning with a wide range of preferred directions and a mean full width at half-maximum of 129 degrees. Analysis of latency using the "receiver operating characteristic" to compare responses to target motion in opposite directions showed that the directional response of 58% of FPA neurons led the initiation of pursuit, while 19% led by 25 ms or more. Analysis of neuronal responses during pursuit of a range of target velocities revealed that the sensitivity to eye velocity was larger during the initiation of pursuit than during the maintenance of pursuit, consistent with two components of firing related to image motion and eye motion. FPA neurons showed correlates of two behavioral features of pursuit documented in prior reports. 1) Eye acceleration at the initiation of pursuit declines as a function of the eccentricity of the moving target. FPA neurons show decreased firing at the initiation of pursuit in parallel with the decline in eye acceleration. This finding is consistent with prior suggestions that the FPA plays a role in modulating the gain of visual-motor transmission for pursuit. 2) A stationary eccentric cue evokes a smooth eye movement opposite in direction to the cue and enhances the pursuit evoked by subsequent target motions. Many pursuit neurons in the FPA showed weak, phasic visual responses for stationary targets and were tuned for the positions about 4 degrees eccentric on the side opposite to the preferred pursuit direction. However, few neurons (12%) responded during the preparation or execution of saccades. The responses to the stationary target could account for the behavioral effects of stationary, eccentric cues. Further analysis of the relationship between firing rate and retinal position error during pursuit in the preferred and opposite directions failed to provide evidence for a large contribution of image position to the firing of FPA neurons. We conclude that FPA processes information in terms of image and eye velocity and that it is functionally separate from the saccadic frontal eye fields, which processes information in terms of retinal image position.     

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.     

A comparison of visual responses to object- and ego-motion in the macaque superior temporal polysensory area

The responses of visual movement-sensitive neurons in the anterior superior temporal polysensory area (STPa) of monkeys were studied during object-motion, ego-motion and during both together. The majority of the cells responded only to the image of a moving object against a stationary background and failed to respond to the retinal movement of the same object (against the same background) caused by the monkey's ego-motion. All the tested cells continued responding to the object-motion during ego-motion in the opposite direction. By contrast, most cells failed to respond to the motion of an object when the observer and object moved at the same speed and direction (eliminating observer-relative motion cues). The results indicate that STPa cells compute motion relative to the observer and suggest an influence of reference signals (vestibular, somatosensory or retinal) in the discrimination of ego- and object-motion. The results extend observations indicating that STPa cells are selective for visual motion originating from the movements of external objects and unresponsive to retinal changes correlated with the observer's own movements.     

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.     

A possible visual pathway to the cat caudate nucleus involving the pulvinar

Electrical stimulation of the thalamic nucleus pulvinar was found to influence unit activity in the feline caudate nucleus. Twenty-six (18.3%) units were encountered, in this subcortical region of the brain, that responded to activation of the pulvinar input in anesthetized cats and 41 (54%) in awake animals. In the two types of experiments, stimulation of the pulvinar induced mainly an initial excitatory reaction (81% and 78% of responsive cells, respectively). A latency analysis indicated that the majority of responses occurred at a long latency, while 9 (34.6%) cells in anesthetized cats and 5 (12%) in awake animals were excited at a short latency. The short latency is compatible with the involvement of a monosynaptic pathway between the pulvinar and the caudate nucleus. Units that responded to thalamic stimulation were found predominantly in the posterior regions of the caudate nucleus. These results confirm previous neuroanatomical findings of a direct projection from the pulvinar to the feline caudate nucleus. In awake animals, neurons activated by pulvinar stimulation were also tested, using visual stimuli of various orientations. Out of 41 units, 63% were classified as having visual responses. Of these, 5 cells were found to respond selectively to a particular orientation of the visual stimulus. Three of these were excited at a short latency by pulvinar stimulation. The possible involvement of a direct pathway from the pulvinar to the caudate nucleus in the processing of visual information is discussed.     

Visuomotor properties of neurons of the anterior suprasylvian gyrus in the awake cat

Summary 1. Single cell activity was recorded from the Anterior Suprasylvian (ASS) gyrus of cats trained to orient their gaze toward visual or auditory stimuli. 2. Sixty-five fixation cells were activated or suppressed as long as the animals were attentive to a particular region of space in the tangential or in the radial direction. Most of these fixation cells were neither light nor sound sensitive. 3. Fifty-five cells were activated in relation to saccades. Fourteen neurons were active before and 41 after the onset of saccades. Nineteen neurons were also active with spontaneous eye movements in the dark. 4. Fifteen neurons were seemingly related to vergence. They were not light-sensitive. They were preferentially activated by visual stimuli moving in the radial direction either towards or away from animal's face. 5. Fifty light-sensitive neurons responded to moving stimuli. Only two neurons responded to onset of eccentric stationary light-stimuli. 6. Fifty-one neurons showed a modulation in relation to vestibular stimulation. A majority showed, in addition, a vestibulo-collic response. These data suggest that the ASS gyrus in cats has a major role in the construction of the behavioral space.     

Neural correlates of reafference: evoked brain activity during motion perception and saccadic eye movements

The ability to perceive a stable visual environment despite eye movements and the resulting displacement of the retinal image is a striking feature of visual perception. In order to study the brain mechanism related to this phenomenon, an EEG was recorded from 30 electrodes spaced over the occipital, temporal and parietal brain areas while stationary or moving visual stimuli with velocities between 178 degrees/s and 533 degrees/s were presented. The visual stimuli were presented both during saccadic eye movements and with stationary eyes. Stimulus-related potentials were measured, and the effects of absolute and relative stimulus velocity were analyzed. Healthy adults participated in the experiments. In all 36 subjects and experimental conditions, four potential components were found with mean latencies of about 70, 140, 220 and 380 ms. The latency of the two largest components between 100 and 240 ms decreased while field strength increased with higher absolute stimulus velocity for both stationary and moving eyes, whereas relative stimulus velocity had no effect on amplitude, latency and topography of the visual evoked potential (VEP) components. If the visual system uses retinal motion information only, we would expect a dependence upon relative velocity. Since field strength and latency of the components were independent of eye movements but dependent upon absolute stimulus velocity, the visual cortex must use extraretinal information to extract stimulus velocity. This was confirmed by the fact that significant topographic changes were observed when brain activity evoked during saccades and with stationary eyes was compared. In agreement with the reafference principle, the findings indicate that the same absolute visual stimulus activates different neuronal elements during saccades than during fixation.     

Activity of eye movement-related neurons in and near the interstitial nucleus of Cajal during sinusoidal vertical linear acceleration and optokinetic stimuli

Summary 1. A total of 43 neurons that showed a close correlation with vertical eye movement with a burst-tonic or tonic type response during spontaneous saccades, were recorded within, and in the close vicinity of, the interstitial nucleus of Cajal (INC) in alert cats. Neuronal responses to sinusoidal vertical linear acceleration (0.2–0.85 Hz, amplitude 10.5 cm) and optokinetic stimuli (0.1–1.0 Hz, amplitude 10.5 cm), were examined. 2. All 43 eye movement-related neurons responded to sinusoidal vertical linear acceleration in the presence of a stationary visual pattern in correlation to robust eye movement responses with compensatory phase. Phase and gain values (re stimulus position) of response of individual cells were independent of the stimulus frequencies tested. Of these, 33 cells were examined during linear acceleration without visual input. Most cells (27/33) did not respond even when a weak linear vestibulo-ocular reflex was present (6/27). The remaining 6 cells (6/33) responded to linear acceleration. Their mean phase values advanced by 80 ° and gain dropped by 55% compared to the responses with visual inputs. 3. Twenty eight of the 43 cells were examined during vertical optokinetic stimuli. The activity of all 28 cells was modulated in correlation to eye movement responses. Response phase showed more lag, and gain decreased as stimulus frequencies increased, similar to optokinetic eye movement responses. 4. The close correlation between the activity of eye movement-related neurons in the INC region and robust eye movements during linear acceleration with visual inputs and optokinetic stimuli suggest that these neurons are involved in some aspect of vertical eye position generation during such stimuli.     

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.     

Perisaccadic mislocalization without saccadic eye movements

Despite frequent saccadic gaze shifts we perceive the surrounding visual world as stable. It has been proposed that the brain uses extraretinal eye position signals to cancel out saccade-induced retinal image motion. Nevertheless, stimuli flashed briefly around the onset of a saccade are grossly mislocalized, resulting in a shift and, under certain conditions, an additional compression of visual space. Perisaccadic mislocalization has been related to a spatio-temporal misalignment of an extraretinal eye position signal with the corresponding saccade. Here, we investigated perceptual mislocalization of human observers both in saccade and fixation conditions. In the latter conditions, the retinal stimulation during saccadic eye movements was simulated by a fast saccade-like shift of the stimulus display. We show that the spatio-temporal pattern of both the shift and compression components of perceptual mislocalization can be surprisingly similar before real and simulated saccades. Our findings suggest that the full pattern of perisaccadic mislocalization can also occur in conditions which are unlikely to involve changes of an extraretinal eye position signal. Instead, we suggest that, under the conditions of our experiments, the arising difficulty to establish a stable percept of a briefly flashed stimulus within a given visual reference frame yields mislocalizations before fast retinal image motion. The availability of visual references appears to exert a major influence on the relative contributions of shift and compression components to mislocalization across the visual field.     

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 motion response properties of neurons in dorsolateral pontine nucleus of alert monkey

1. In this study we sought to characterize the visual motion processing that exists in the dorsolateral pontine nucleus (DLPN) and make a comparison with the reported visual responses of the middle temporal (MT) and medial superior temporal (MST) areas of the monkey cerebral cortex. The DLPN is implicated as a component of the visuomotor interface involved with the regulation of smooth-pursuit eye movements, because it is a major terminus for afferents from MT and MST and also the source of efferents to cerebellar regions involved with eye-movement control. 2. Some DLPN cells were preferentially responsive to discrete (spot and bar) visual stimuli, or to large-field, random-dot pattern motion, or to both discrete and large-field visual motion. The results suggest differential input from localized regions of MT and MST. 3. The visual-motion responses of DLPN neurons were direction selective for 86% of the discrete visual responses and 95% of the large-field responses. Direction tuning bandwidths (full-width at 50% maximum response amplitude) averaged 107 degrees and 120 degrees for discrete and large-field visual motion responses, respectively. For the two visual response types, the direction index averaged 0.95 and 1.02, indicating that responses to stimuli moving in preferred directions were, on average, 20 and 50 times greater than responses to discrete or large-field stimulus movement in the opposite directions, respectively. 4. Most of the DLPN visual responses to movements of discrete visual stimuli exhibited increases in amplitude up to preferred retinal image speeds between 20 and 80 degrees/s, with an average preferred speed of 39 degrees/s. At higher speeds, the response amplitude of most units decreased, although a few units exhibited a broad saturation in response amplitude that was maintained up to at least 150 degrees/s before the response decreased. Over the range of speeds up to the preferred speeds, the sensitivity of DLPN neurons to discrete stimulus-related, retinal-image speed averaged 3.0 spikes/s per deg/s. The responses to large-field visual motion were less sensitive to retinal image speed and exhibited an average sensitivity of 1.4 spikes/s per deg/s before the visual response saturated. 5. DLPN and MT were quantitatively comparable with respect to degree of direction selectivity, retinal image speed tuning, and distribution of preferred speeds. Many DLPN receptive fields contained the fovea and were larger than those of MT and more like MST receptive fields in size.(ABSTRACT TRUNCATED AT 400 WORDS)     

Visual tracking neurons in primate area MST are activated by smooth-pursuit eye movements of an "imaginary" target

Because smooth-pursuit eye movements (SPEM) can be executed only in the presence of a moving target, it has been difficult to attribute the neuronal activity observed during the execution of these eye movements to either sensory processing or to motor preparation or execution. Previously, we showed that rhesus monkeys can be trained to perform SPEM directed toward an "imaginary" target defined by visual cues confined to the periphery of the visual field. The pursuit of an "imaginary" target provides the opportunity to elicit SPEM without stimulating visual receptive fields confined to the center of the visual field. Here, we report that a subset of neurons [85 "imaginary" visual tracking (iVT)-neurons] in area MST of 3 rhesus monkeys were identically activated during pursuit of a conventional, foveal dot target and the "imaginary" target. Because iVT-neurons did not respond to the presentation of a moving "imaginary" target during fixation of a stationary dot, we are able to exclude that responses to pursuit of the "imaginary" target were artifacts of stimulation of the visual field periphery. Neurons recorded from the representation of the central parts of the visual field in neighboring area MT, usually vigorously discharging during pursuit of foveal targets, in no case responded to pursuit of the "imaginary" target. This dissociation between MT and MST neurons supports the view that pursuit responses of MT neurons are the result of target image motion, whereas those of iVT-neurons in area MST reflect an eye movement-related signal that is nonretinal in origin. iVT-neurons fell into two groups, depending on the properties of the eye movement-related signal. Whereas most of them (71%) encoded eye velocity, a minority showed responses determined by eye position, irrespective of whether eye position was changed by smooth pursuit or by saccades. Only the former group exhibited responses that led the eye movement, which is a prerequisite for a causal role in the generation of SPEM.     

Predictive responses of periarcuate pursuit neurons to visual target motion

The smooth pursuit eye movement system uses retinal information about the image-slip-velocity of the target in order to match the eye-velocity-in-space (i.e., gaze-velocity) to the actual target velocity. To maintain the target image on the fovea during smooth gaze tracking, and to compensate for the long delays involved in processing visual motion information and/or eye velocity commands, the pursuit system must use prediction. We have shown recently that both retinal image-slip-velocity and gaze-velocity signals are coded in the discharge of single pursuit-related neurons in the simian periarcuate cortex. To understand how periarcuate pursuit neurons are involved in predictive smooth pursuit, we examined the discharge characteristics of these neurons in trained Japanese macaques. When a stationary target abruptly moved sinusoidally along the preferred direction at 0.5 Hz, the response delays of pursuit cells seen at the onset of target motion were compensated in succeeding cycles. The monkeys were also required to continue smooth pursuit of a sinusoidally moving target while it was blanked for about half of a cycle at 0.5 Hz. This blanking was applied before cell activity normally increased and before the target changed direction. Normalized mean gain of the cells' responses (re control value without blanking) decreased to 0.81(+/-0.67 SD), whereas normalized mean gain of the eye movement (eye gain) decreased to 0.65 (+/-0.16 SD). A majority (75%) of pursuit neurons discharged appropriately up to 500 ms after target blanking even though eye velocity decreased sharply, suggesting a dissociation of the activity of those pursuit neurons and eye velocity. To examine whether pursuit cell responses contain a predictive component that anticipates visual input, the monkeys were required to fixate a stationary target while a second test laser spot was moved sinusoidally. A majority (68%) of pursuit cells tested responded to the second target motion. When the second spot moved abruptly along the preferred direction, the response delays clearly seen at the onset of sinusoidal target motion were compensated in succeeding cycles. Blanking (400-600 ms) was also applied during sinusoidal motion at 1 Hz before the test spot changed its direction and before pursuit neurons normally increased their activity. Preferred directions were similar to those calculated for target motion (normalized mean gain=0.72). Similar responses were also evoked even if the second spot was flashed as it moved. Since the monkeys fixated the stationary spot well, such flashed stimuli should not induce significant retinal slip. These results taken together suggest that the prediction-related activity of periarcuate pursuit neurons contains extracted visual components that reflect direction and speed of the reconstructed target image, signals sufficient for estimating target motion. We suggest that many periarcuate pursuit neurons convey this information to generate appropriate smooth pursuit eye movements.     

MST neuronal responses to heading direction during pursuit eye movements

As you move through the environment, you see a radial pattern of visual motion with a focus of expansion (FOE) that indicates your heading direction. When self-movement is combined with smooth pursuit eye movements, the turning of the eye distorts the retinal image of the FOE but somehow you still can perceive heading. We studied neurons in the medial superior temporal area (MST) of monkey visual cortex, recording responses to FOE stimuli presented during fixation and smooth pursuit eye movements. Almost all neurons showed significant changes in their FOE selective responses during pursuit eye movements. However, the vector average of all the neuronal responses indicated the direction of the FOE during both fixation and pursuit. Furthermore, the amplitude of the net vector increased with increasing FOE eccentricity. We conclude that neuronal population encoding in MST might contribute to pursuit-tolerant heading perception.