Response properties of single units in the lateral terminal nucleus of the accessory optic system in the behaving primate

1. To determine the potential role of the primate accessory optic system (AOS) in optokinetic and smooth-pursuit eye movements, we recorded the activity of 110 single units in a subdivision of the AOS, the lateral terminal nucleus (LTN), in five alert rhesus macaques. All monkeys were trained to fixate a stationary target spot during visual testing and to track a small spot moving in a variety of visual environments. 2. LTN units formed a continuum of types ranging from purely visual to purely oculomotor. Visual units (50%) responded best for large-field (70 x 50 degrees), moving visual stimuli and had no response associated with smooth-pursuit eye movement; some responded during smooth pursuit in the dark, but the response disappeared if the target was briefly extinguished, indicating that their smooth-pursuit-related response reflected activation of a parafoveal receptive field. Eye movement and visual units (36%) responded both for large, moving visual stimuli and during smooth-pursuit eye movements made in the dark. Eye movement units (14%) discharged during smooth-pursuit or other eye movements but showed no evidence of visual sensitivity. 3. Essentially all (98%) LTN units were direction selective, responding preferentially during vertical background and/or smooth-pursuit movement. The vast majority (88%) preferred upward background and/or eye movement. During periodic movement of the large-field visual background while the animal fixated, their firing rates were modulated above and below rather high resting rates. Although LTN units typically responded best to movement of large-field stimuli, some also responded well to small moving stimuli (0.25 degrees diam). 4. LTN units could be separated into two populations according to their dependence on visual stimulus velocity. For periodic triangle wave stimuli, both types had velocity thresholds less than 3 degrees/s. As stimulus velocity increased above threshold, the activity of one type reached peak firing rates over a very narrow velocity range and remained nearly at peak firing for velocities from approximately 4-80 degrees/s. The firing rates of the other type exhibited velocity tuning in which the firing rate peaked at an average preferred velocity of 13 degrees/s and decreased for higher velocities. 5. A close examination of firing rates to sinusoidal background stimuli revealed that both unit types exhibited unusual behaviors at the extremes of stimulus velocity.(ABSTRACT TRUNCATED AT 400 WORDS)     

Response properties of dorsolateral pontine units during smooth pursuit in the rhesus macaque

1. The anatomical connections of the dorsolateral pontine nucleus (DLPN) implicate it in the production of smooth-pursuit eye movements. It receives inputs from cortical structures believed to be involved in visual motion processing (middle temporal cortex) or motion execution (posterior parietal cortex) and projects to the flocculus of the cerebellum, which is involved in smooth pursuit. To determine the role of the DLPN in smooth pursuit, we have studied the discharge patterns of 191 DLPN neurons in five monkeys trained to make smooth-pursuit eye movements of a spot moving either across a patterned background or in darkness. 2. Four unit types could be distinguished. Visual units (15%) discharged in response to movement of a large textured pattern, often in a direction-selective fashion but not during smooth pursuit of a spot in the dark. Eye movement neurons (31%) discharged during sinusoidal smooth pursuit in the dark with peak discharge rate either at peak eye position or peak eye velocity, but they showed no response during background movement or during other visual stimulation. These units continued to discharge when the target was extinguished (blanked) briefly, and the monkey continued to make smooth eye movements in the dark. The majority (54%) of our DLPN units discharged during both smooth pursuit in the dark and background movement while the monkey fixated. Blanking the target during smooth pursuit revealed that these units fell into two distinct classes. Visual pursuit units ceased discharging during a blank, suggesting that they had only a visual sensitivity. Pursuit and visual units continued to discharge during the blank, indicating that they had a combined oculomotor and visual sensitivity. 3. Ninety-five percent of the units that discharged during smooth pursuit were direction selective. These units had rather broad directional tuning curves with widths at half height ranging from 65 to 180 degrees. Many preferred directions for DLPN units were observed, although the vertical and near-vertical directions predominated. 4. Most units that responded to large-field background movement were direction selective. During sinusoidal movement of a large-field background, half of them also discharged in relation to stimulus velocity, whereas others did not.     

Role of the pretectal nucleus of the optic tract in short-latency ocular following responses in monkeys

When a large-field image is suddenly moved in front of an observer, an ocular following response (OFR) with short latency (<60 ms in monkey and <85 ms in human) is observed. Previous studies have shown that neurons in the pretectal nucleus of the optic tract (NOT) of the monkey respond to movements of large-field visual stimuli. To understand the potential role of the NOT in the OFR, we first recorded single-unit activity in the NOT of four monkeys (Macaca fuscata). Sixty-six NOT neurons preferred large-field ipsiversive visual motion. In 86% (49/57) of the neurons, optimal directions were distributed over +/-30 degrees from ipsilateral. NOT units were sensitive to the speed of the visual motion; 54% (27/50) preferred slow (< or =20 degrees/s), 22% (11/50) preferred fast (> or =80 degrees/s) and the remainder intermediate speeds. Their response latencies to the moving visual scene were very short (approximately 51 ms), and 44% of them led the onset of the OFR by 10 ms or more. To characterize the response properties of these neurons, we reconstructed the temporal firing patterns of 17 NOT neurons, using the acceleration, velocity, position and bias components of retinal image slip or eye movements during the OFR by a least squares error method. For each stimulus speed fitting condition, using either retinal slip or eye movements, their firing patterns were matched to some extent although the goodness of fit was better using retinal slip than when eye movements were used. Neither of these models could be applied independently of stimulus speed, suggesting that the firing pattern of the NOT neurons represented information associated with retinal slip or eye movements during the OFR, over a limited range. To provide further evidence that the NOT is involved in generating the OFR, we placed unilateral microinjections of muscimol into the NOT. Following the muscimol injection, we observed a approximately 50% decrease in eye velocity of the OFR toward the side of injection regardless of stimulus speed, while only a weak effect was observed in the OFR during contraversive or vertical image motion. These results suggest that the NOT may play a role in the initiation and support of the short-latency ocular following response.     

Responses of monkey nucleus of the optic tract neurons during pursuit and fixation.

We recorded 101 neurons in the nucleus of the optic tract (NOT) of 3 rhesus monkeys. The neurons were tested in a variety of oculomotor paradigms. This report focusses on the modulation of NOT neuronal activity during smooth pursuit eye movements. A small horizontally moving spot (less than 1 degrees) elicited a directionally specific response during fixation and revealed thereby the extent of the receptive fields. During pursuit NOT neurons are coding for target slip. If eye speed exceeds target speed the direction of retinal slip is reversed and in accordance with their directional sensitivity NOT neurons immediately change their activity. This result proves the slip transfer function as well as the independence from eye movement signals of NOT neurons. During pursuit across a structured background some neurons are still coding for target slip whereas other neurons are coding for background slip. These two groups of neurons can also be distinguished by their response during fixation. The response of a target slip neuron to a background movement is cancelled, whereas the response of a background neuron is not affected by fixation. There is no difference in size of receptive fields for these two groups of neurons. We conclude from our findings that directionally selective cells in the monkey NOT may provide input to the pursuit system as well as to the optokinetic system. This dichotomy may also be reflected in different efferent projections: to the nucleus reticularis tegmenti pontis and to the inferior olive, respectively. A similar notion was introduced by the late Maekawa for the rabbit's NOT.     

Further evidence for selective difficulty of upward eye pursuit in juvenile monkeys: effects of optokinetic stimulation, static roll tilt, and active head movements

The smooth-pursuit system moves the eyes in space accurately to track slowly moving objects of interest despite visual inputs from the moving background and/or vestibular inputs during head movements. Recently, our laboratory has shown that young primates exhibit asymmetric eye movements during vertical pursuit across a textured background; upward eye velocity gain is reduced. To further understand the nature of this asymmetry, we performed three series of experiments in young monkeys. In Experiment 1, we examined whether this asymmetry was due to an un-compensated downward optokinetic reflex induced by the textured background as it moves across the retina in the opposite direction of the pursuit eye movements. For this, we examined the monkeys’ ability to fixate a stationary spot in space during movement of the textured background and compared it with vertical pursuit across the stationary textured background. We also examined gains of optokinetic eye movements induced by downward motion of the textured background during upward pursuit. In both task conditions, gains of downward eye velocity induced by the textured background were too small to explain reduced upward eye velocity gains. In Experiment 2, we examined whether the frame of reference for low-velocity, upward pursuit was orbital or earth vertical. To test this, we first applied static tilt in the roll plane until the animals were nearly positioned on their side in order to dissociate vertical or horizontal eye movements in the orbit from those in space. Deficits were observed for upward pursuit in the orbit but not in space. In Experiment 3, we tested whether asymmetry was observed during head-free pursuit that requires coordination between eye and head movements. Asymmetry in vertical eye velocity gains was still observed during head-free pursuit although it was not observed in vertical head velocity. These results, taken together, suggest that the asymmetric eye movements during vertical pursuit are specific for upward, primarily eye pursuit in the orbit.     

The function of the cerebellar uvula in monkey during optokinetic and pursuit eye movements: single-unit responses and lesion effects

The cerebellum is known to participate in visually guided eye movements. The cerebellar uvula receives projections from pontine nuclei that have been implicated in visual motion processing and the generation of smooth pursuit. Single-unit and lesion studies were conducted to determine how the uvula might further process these input signals. Purkinje cells and input fibers were recorded during a variety of visual and oculomotor paradigms. Most Purkinje cells were modulated in either an excitatory or inhibitory fashion by prolonged, horizontal optokinetic drum rotation. A small proportion of cells responded during smooth tracking of a small spot of light. As a paradox to the physiological data, lesions of the uvula produced a profound effect on smooth-pursuit eye movements. Initial eye velocity for pursuit in the direction contraversive to the lesion site was increased substantially following lesions in comparison with prelesion controls. The lesions also affected optokinetic nystagmus in the direction contraversive to the lesion, but not as drastically as they did pursuit. Overall the results suggest that the uvula is not in the neuronal pathway that directly controls pursuit, but instead serves to adjust the gain of this system as a result of abnormal periods of motion of the visual world.     

Posterior vermal Purkinje cells in macaques responding during saccades, smooth pursuit, chair rotation and/or optokinetic stimulation.

Anatomical locations of the Purkinje cells (P cells), showing modulations in activity during either saccadic or smooth-pursuit eye movements, during primate chair rotation, or in response to optokinetic stimulation, were studied in the posterior vermes of monkeys trained to move their eyes with a visual target. The majority (68.3%) of the responsive P cells were saccade-related units. They were located exclusively in vermal lobules VIc and VII: the oculomotor vermis. Most P cells sensitive to chair rotation were located in vermal lobules VIa,b and VIII (91.2%), designated as the paraoculomotor vermis. The P cells which modulated activity during smooth-pursuit eye movements, associated with eye position, or during optokinetic stimulation were found in both the oculomotor and paraoculomotor vermis. There were 25 P cells which modulated their activity during smooth pursuit in the oculomotor vermis. Among them, only three responded also to optokinetic stimulation but none was sensitive to chair-rotation stimulation. These findings suggest that the control of saccadic eye movements is the primary function of the oculomotor vermis.     

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)     

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)     

Smooth-pursuit eye movement deficits with chemical lesions in the dorsolateral pontine nucleus of the monkey

1. Anatomical and single-unit recording studies suggest that the dorsolateral pontine nucleus (DLPN) in monkey is a major link in the projection of descending visual motion information to the cerebellum. Such studies coupled with cortical and cerebellar lesion results suggest a major role for this basilar pontine region in the mediation of smooth-pursuit eye movements. 2. To provide more direct evidence that this pontine region is involved in the control of smooth-pursuit eye movements, focal chemical lesions were made in DLPN in the vicinity of previously recorded visual motion and pursuit-related neurons. Eye movement responses were subsequently recorded in these lesioned animals under several behavioral paradigms. 3. A major deficit in smooth-pursuit performance was produced after unilateral DLPN lesions generated either reversibly with lidocaine or more permanently with ibotenic acid. Pursuit impairments were observed during steady-state tracking of sinusoidal target motion as well as during the initiation of pursuit tracking to sudden ramp target motion. Through the use of the latter technique, initial eye acceleration was reduced to less than one-half of normal for animals with large lesions of the dorsolateral and lateral pontine nuclei. 4. The pursuit deficit in all animals was directional in nature and was not dependent on the visual hemifield in which the motion stimulus occurred. The largest effect for horizontal tracking occurred in all animals for pursuit directed ipsilateral to the lesion. Animals also showed major deficits in one or both directions of vertical pursuit, although the primary direction of the vertical impairment was variable from animal to animal. 5. Chemical lesions in the DLPN also produced comparable deficits in the initiation of optokinetic-induced smooth eye movements in the ipsilateral direction. In contrast to this effect on the initial optokinetic response, in the one lesioned animal studied during prolonged constant velocity optokinetic drum rotation, smooth eye speed increased slowly over a 10- to 15-s period to reach a level that closely matched drum speed. These results suggest that pathways outside the DLPN can generate the steady-state optokinetic response. 6. Saccades to stationary targets were normal after DLPN lesions, but corrective saccades made to targets moving in the direction ipsilateral to the lesion were much more hypometric than similar prelesion control saccades. 7. The pursuit deficits produced by lidocaine injections recovered within 30 min. The ibotenic acid deficits were maximal approximately 1 day after the injection and recovered rapidly thereafter over a time period of 3-7 days.(ABSTRACT TRUNCATED AT 400 WORDS)     

Purkinje cells of the cerebellar dorsal vermis: simple-spike activity during pursuit and passive whole-body rotation

To track a slowly moving object during whole body rotation, smooth-pursuit and vestibularly induced eye movements must interact to maintain the accuracy of eye movements in space (i.e., gaze), and gaze movement signals must eventually be converted into eye movement signals in the orbit. To understand the role played by the cerebellar vermis in pursuit-vestibular interactions, in particular whether the output of the vermis codes gaze-velocity or eye-velocity, we examined simple-spike activity of 58 Purkinje (P-) cells in lobules VI-VII of head-stabilized Japanese monkeys that were trained to elicit smooth-pursuit eye movements and cancel their vestibuloocular reflex (VOR) during passive whole body rotation around horizontal, vertical, or oblique axes. All pursuit-sensitive vermal P-cells also responded during VOR cancellation, and the majority of them had peak modulation near peak stimulus velocity. The directions of maximum modulation during these two tasks were distributed in all directions with a downward preponderance. Using standard criteria, 40% of pursuit-sensitive vermal P-cells were classified as gaze-velocity. Other P-cells were classified either as eye/head-velocity group I (36%) that had similar preferred directions during pursuit and VOR cancellation but that had larger responses during VOR x1 when gaze remained stationary, or as eye/head-velocity group II (24%) that had oppositely directed or orthogonal eye and head movement sensitivity during pursuit and VOR cancellation. Eye/head-velocity group I P-cells contained cells whose activity was correlated with eye velocity. Modulation of many P-cells of the three groups during VOR x1 could be accounted for by the linear addition of their modulations during pursuit and VOR cancellation. When monkeys fixated a stationary target, over half of the P-cells tested, including gaze-velocity P-cells, discharged in proportion to the velocity of retinal motion of a second spot. These observations are in a striking contrast to our previous results for floccular vertical P-cells. Because we used identical tasks, these differences suggest that the two cerebellar regions are involved in very different kinds of processing of pursuit-vestibular interactions.     

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.     

A quantitative analysis of the direction-specific response of neurons in the cat's nucleus of the optic tract

Summary All cells in the nucleus of the optic tract (NOT) of the cat, that Bcould be activated antidromically from the inferior olive, were shown to be direction-specific, as influenced by horizontal movements of an extensive visual stimulus. Cells in the left NOT were activated by leftward and inhibited by rightward movement, while those in the right NOT were activated by rightward and inhibited by leftward movement. Vertical movements did not modulate the spontaneous activity of the cells. The mean spontaneous discharge rate in 50 NOT cells was 30 spikes/s.This direction-specific response was maintained over a broad velocity range (<0.1 ° – >100 °/s). Velocities over 200 °/s could inhibit NOT cells regardless of stimulus direction.All cells in the NOT were driven by the contralateral eye, about half of them by the ipsilateral eye also. In addition, activation through the contralateral eye was stronger in most binocular units. Binocular cells preferred the same direction in the visual space through both eyes.An area approximately corresponding to the visual streak in the cat's retina projected most densely onto NOT cells. This included an extensive ipsilateral projection. No clear retinotopic order was seen. The most sensitive zone in the very large receptive fields (most diameters being >20 °) was along the horizontal zero meridian of the visual field.The retinal input to NOT cells was mediated by W-fibers.The striking similarities between the input characteristics of NOT-cells and optokinetic nystagmus are discussed. The direction selectivity and ocular dominance of the NOT system as a whole can provide a possible explanation for the directional asymmetry in the cat's optokinetic nystagmus when only one eye is stimulated.This work was supported by DFG-Grants No 450/3 and 450/7 to K.-P. Hoffmann     

Visual and vergence eye movement-related responses of pursuit neurons in the caudal frontal eye fields to motion-in-depth stimuli

The caudal parts of the frontal eye fields (FEF) contain smooth-pursuit related neurons. Previous studies show that most FEF pursuit neurons carry visual signals in relation to frontal spot motion and discharge before the initiation of smooth-pursuit. It has also been demonstrated that most FEF pursuit neurons discharge during vergence tracking. Accurate vergence tracking requires information about target motion-in-depth. To further understand the role of the FEF in vergence tracking and to determine whether FEF pursuit neurons carry visual information about target motion-in-depth, we examined visual and vergence eye movement-related responses of FEF pursuit neurons to sinusoidal spot motion-in-depth. During vergence tracking, most FEF pursuit neurons exhibited both vergence eye position and velocity sensitivity. Phase shifts (re target velocity) of most neurons remained virtually constant up to 1.5 Hz. About half of FEF pursuit neurons exhibited visual responses to spot motion-in-depth. The preferred directions for visual responses of most neurons were similar to those during vergence tracking. Visual responses of most of these neurons exhibited sensitivity to the velocity of spot motion-in-depth. Phase shifts of most of the responding neurons remained virtually constant up to 2.0 Hz. Neurons that exhibited visual responses in-depth were mostly separate from neurons that showed visual responses in the frontal plane. To further examine whether FEF pursuit neurons could participate in initiation of vergence tracking, we examined latencies of neuronal responses with respect to vergence eye movements induced by step target motion-in-depth. About half of FEF pursuit neurons discharged before the onset of vergence eye movements with lead times longer than 20 ms. These results together with previous observations suggest that the caudal FEF carries visual signals appropriate to be converted into motor commands for pursuit in depth and frontal plane.     

Fastigial nucleus activity in the alert monkey during slow eye and head movements

1. Single units were recorded extracellularly from the fastigial nucleus of three macaque monkeys. Two untrained animals were subjected to whole-body yaw rotations in the light and dark and to full-field horizontal optokinetic stimuli provided by a drum with vertical stripes. The third also was subjected to sinusoidal yaw rotations but, in addition, was trained to follow a small spot, which moved in various ways relative to the animal, to reveal possible smooth pursuit and vestibular sensitivities. 2. On the basis of their responses to vestibular and optokinetic stimuli and their responses during smooth pursuit, fastigial neurons could be divided functionally into a rostral and a caudal group. 3. Most rostral neurons exhibited an increased firing for contralateral head rotations and ipsilateral optokinetic stimuli. A few had the opposite combination of directional preferences. The average firing rates increased monotonically both with contralateral head velocity and ipsilateral drum velocity and decreased monotonically for the oppositely directed movements. There was no change in firing rate for either spontaneous saccades or smooth pursuit of a small moving spot. 4. In contrast, neurons in the caudal fastigial nuclei not only have a robust vestibular sensitivity, but respond during smooth pursuit as well. Most discharge during contralateral head velocity and contralateral smooth pursuit so that they exhibit very little modulation during the vestibuloocular reflex (VOR) or when the rotating animal is fixating a target stationary in the world (SIW). The remaining neurons discharge during contralateral head rotations but ipsilateral eye rotations; these units exhibit their greatest modulation during the SIW condition. 5. Because they respond during quite different behavioral situations, it seems likely that rostral fastigial neurons are involved with descending control of the somatic musculature, whereas the caudal neurons are involved in oculomotor control. The sparse anatomic and lesion data that is available is consistent with this idea.     

Pursuit-related neurons in the supplementary eye fields: discharge during pursuit and passive whole body rotation

The primate frontal cortex contains two areas related to smooth-pursuit: the frontal eye fields (FEFs) and supplementary eye fields (SEFs). To distinguish the specific role of the SEFs in pursuit, we examined discharge of a total of 89 pursuit-related neurons that showed consistent modulation when head-stabilized Japanese monkeys pursued a spot moving sinusoidally in fronto-parallel planes and/or in depth and with or without passive whole body rotation. During smooth-pursuit at different frequencies, 43% of the neurons tested (17/40) exhibited discharge amplitude of modulation linearly correlated with eye velocity. During cancellation of the vestibulo-ocular reflex and/or chair rotation in complete darkness, the majority of neurons tested (91% = 30/33) responded. However, only 17% of the responding neurons (4/30) were modulated in proportion to gaze (eye-in-space) velocity during pursuit-vestibular interactions. When the monkeys fixated a stationary spot, 20% of neurons tested (7/34) responded to motion of a second spot. Among the neurons tested for both smooth-pursuit and vergence tracking (n = 56), 27% (15/56) discharged during both, 62% (35/56) responded during smooth-pursuit only, and 11% (6/56) during vergence tracking only. Phase shifts (relative to stimulus velocity) of responding neurons during pursuit in frontal and depth planes and during chair rotation remained virtually constant (< or =1 Hz). These results, together with the robust vestibular-related discharge of most SEF neurons, show that the discharge of the majority of SEF pursuit-related neurons is quite distinct from that of caudal FEF neurons in identical task conditions, suggesting that the two areas are involved in different aspects of pursuit-vestibular interactions including predictive pursuit.     

Effects of early monocular deprivation on visual input to cat nucleus of the optic tract

Single cells were recorded extracellularly in the nucleus of the optic tract (NOT) in monocularly deprived cats. Monocular deprivation had no effect on the direction specificity of these neurons, i.e. all cells in the left nucleus preferred movements from right to left and all units in the right nucleus preferred movements from left to right in the visual field. Neurons driven from the deprived eye failed to respond to stimuli moving at velocities above 10 degrees/s whereas neurons driven from the non-deprived eye responded to velocities up to and above 100 degrees/s as do neurons in normal cats. In 8 out of the 10 cats tested all cells in the two nuclei could be influenced only from the contralateral eye irrespective whether this was the deprived or the non-deprived eye. In the other two cats the influence from the non-deprived eye on cells in the ipsilateral NOT was found to be normal. This influence is mediated probably via cortico-fugal projections. In the 8 abnormal cats a clear deprivation effect could be assigned for the first time to the non-deprived eye consisting in a loss of its connections to the ipsilateral NOT. Electrical stimulation of the visual cortex revealed, however, the existence of a connection between the visual cortex and the NOT. A possible explanation for the specific deficit with visual stimulation in the cortico-pretectal synapse ipsilateral to the non-deprived eye is discussed in relation to developmental mechanisms. The conduction velocity of retinal input to the NOT and the output of the NOT to the inferior olive remained uninfluenced by visual deprivation.     

Cue-dependent memory-based smooth-pursuit in normal human subjects: importance of extra-retinal mechanisms for initial pursuit

Using a cue-dependent memory-based smooth-pursuit task previously applied to monkeys, we examined the effects of visual motion-memory on smooth-pursuit eye movements in normal human subjects and compared the results with those of the trained monkeys. These results were also compared with those during simple ramp-pursuit that did not require visual motion-memory. During memory-based pursuit, all subjects exhibited virtually no errors in either pursuit-direction or go/no-go selection. Tracking eye movements of humans and monkeys were similar in the two tasks, but tracking eye movements were different between the two tasks; latencies of the pursuit and corrective saccades were prolonged, initial pursuit eye velocity and acceleration were lower, peak velocities were lower, and time to reach peak velocities lengthened during memory-based pursuit. These characteristics were similar to anticipatory pursuit initiated by extra-retinal components during the initial extinction task of Barnes and Collins (J Neurophysiol 100:1135–1146, 2008b). We suggest that the differences between the two tasks reflect differences between the contribution of extra-retinal and retinal components. This interpretation is supported by two further studies: (1) during popping out of the correct spot to enhance retinal image-motion inputs during memory-based pursuit, pursuit eye velocities approached those during simple ramp-pursuit, and (2) during initial blanking of spot motion during memory-based pursuit, pursuit components appeared in the correct direction. Our results showed the importance of extra-retinal mechanisms for initial pursuit during memory-based pursuit, which include priming effects and extra-retinal drive components. Comparison with monkey studies on neuronal responses and model analysis suggested possible pathways for the extra-retinal mechanisms.     

Initiation of smooth-pursuit eye movements to first-order and second-order motion stimuli

Since normal human subjects can perform smooth-pursuit eye movements only in the presence of a moving target, the occurrence of these eye movements represents an ideal behavioural probe to monitor the successful processing of visual motion. It has been shown previously that subjects can execute smooth-pursuit eye movements to targets defined by luminance and colour, the first-order stimulus attributes, as well as to targets defined by derived, second-order stimulus attributes such as contrast, flicker or motion. In contrast to these earlier experiments focusing on steady-state pursuit, the present study addressed the course of pre-saccadic pursuit initiation (less than 100 ms), as this early time period is thought to represent open-loop pursuit, i.e. the eye movements are exclusively driven by visual inputs proceeding the onset of the eye movement itself. Eye movements of five human subjects tracking first- and second-order motion stimuli had been measured. The analysis of the obtained eye traces revealed that smooth-pursuit eye movements could be initiated to first-order as well as second-order motion stimuli, even before the execution of the first initial saccade. In contrast to steady-state pursuit, the initiation of pursuit was not exclusively determined by the movement of the target, but rather due to an interaction between dominant first-order and less-weighted second-order motion components. Based on our results, two conclusions may be drawn: first and specific for initiation of smooth-pursuit eye movements, we present evidence supporting the notion that initiation of pursuit reflects integration of all available visual motion information. Second and more general, our results further support the hypothesis that the visual system consists of more than one mechanism for the extraction of first-order and second-order motion.     

Smooth-pursuit eye-movement-related neuronal activity in macaque nucleus reticularis tegmenti pontis

Neuronal responses that were observed during smooth-pursuit eye movements were recorded from cells in rostral portions of the nucleus reticularis tegmenti pontis (rNRTP). The responses were categorized as smooth-pursuit eye velocity (78%) or eye acceleration (22%). A separate population of rNRTP cells encoded static eye position. The sensitivity to pursuit eye velocity averaged 0.81 spikes/s per degrees /s, whereas the average sensitivity to pursuit eye acceleration was 0.20 spikes/s per degrees /s(2). Of the eye-velocity cells with horizontal preferences for pursuit responses, 56% were optimally responsive to contraversive smooth-pursuit eye movements and 44% preferred ipsiversive pursuit. For cells with vertical pursuit preferences, 61% preferred upward pursuit and 39% preferred downward pursuit. The direction selectivity was broad with 50% of the maximal response amplitude observed for directions of smooth pursuit up to +/-85 degrees away from the optimal direction. The activities of some rNRTP cells were linearly related to eye position with an average sensitivity of 2.1 spikes/s per deg. In some cells, the magnitude of the response during smooth-pursuit eye movements was affected by the position of the eyes even though these cells did not encode eye position. On average, pursuit centered to one side of screen center elicited a response that was 73% of the response amplitude obtained with tracking centered at screen center. For pursuit centered on the opposite side, the average response was 127% of the response obtained at screen center. The results provide a neuronal rationale for the slow, pursuit-like eye movements evoked with rNRTP microstimulation and for the deficits in smooth-pursuit eye movements observed with ibotenic acid injection into rNRTP. More globally, the results support the notion of a frontal and supplementary eye field-rNRTP-cerebellum pathway involved with controlling smooth-pursuit eye movements.