Integration of retinal and motor signals of eye movements in striate cortex cells of the alert cat

Responses of saccade-depressed (SD) and saccade-excited (SE) cells in the striate cortex to eye movements of alert cats under presentation of a visual pattern were studied under reinforcement of the eye movements with rewards of water. These responses were compared to those on passive displacement of the visual pattern reproducing the movements of the retinal image occurring during eye movements while eye movements were suppressed by withdrawal of reinforcement. Passive displacement of the visual pattern produced in the SD cells depression closely resembled the depression occurring during eye movements under presentation of the visual pattern, in time course as well as in amplitude. Both the saccade depression and the depression due to passive movement of the visual pattern were nonselective to the direction of eye movements. Saccade excitation of the SE cells frequently contained two components occurring at 20 and 80 ms after the onsets of eye movements. Passive displacement of the visual pattern produced in the SE cells excitation comparable with the early component of the saccade excitation. These findings suggest that saccade depression in the SD cells and the early component of the saccade excitation in the SE cells are related to retinal reafference of eye movement. During presentation of visual patterns, saccade excitation in the SE cells was closely related to parameters of eye movements, such as direction, amplitude, duration, and velocity. The correlations were completely lost or strongly reduced in darkness. Lines of evidence were provided that the saccade excitation of the SE cells in darkness or the later component of the saccade excitation under presentation of a visual pattern represents efference copy signals of eye movement transferred to the striate cortex through the Clare-Bishop (CB) cortex. Excitation comparable with saccade excitation in darkness occurred in synchrony with activities of the oculomotor nuclei even after retrobulbar paralysis of eye movement, indicating that the excitation is related to efference copy signals rather than proprioceptive reafference of eye movement.(ABSTRACT TRUNCATED AT 400 WORDS)     

The directional effects of passive eye movement on the directional visual responses of single units in the pigeon optic tectum

 We have investigated the visual responses of 184 single units located in the superficial layers of the optic tectum (OT) of the decerebrate, paralysed pigeon. Visual responses were similar to those reported in non-decerebrate preparations; most units responded best to moving visual stimuli, 18% were directionally selective (they had a clear preference for a particular direction of visual stimulus movement), 76% were plane-selective (they responded to movement in either direction in a particular plane). However, we also found that a high proportion of units showed some sensitivity to the orientation of visual stimuli. We examined the effects of extraocular muscle (EOM) afferent signals, induced by passive eye movement (PEM), on the directional visual responses of units. Visual responses were most modified by particular directions of eye movement, although there was no unique relationship between the direction of visual stimulus movement to which an individual unit responded best and the direction of eye movement that caused the greatest modification of that visual response. The results show that EOM afferent signals, carrying information concerning the direction of eye movement, reach the superficial layers of the OT in the pigeon and there modify the visual responses of units in a manner that suggests some role for these signals in the processing of visual information. Received: 17 June 1996 / Accepted: 29 April 1997     

Input from proprioceptors in the extrinsic ocular muscles to the vestibular nuclei in the giant toad,Bufo marinus

Summary Extracellular unit records were made from the left brain stem of decerebrate, paralysed giant toads (Bufo marinus) during passive movement of the ipsilateral eye. Units in the vestibular nuclear complex (VN) were identified by their short-latency responses to electrical stimulation of the anterior branch of the ipsilateral VIII cranial nerve.Of 58 units in the region of VN, as judged from field potentials to VIII nerve stimulation, fourteen gave phasic excitatory responses to passive movement of the eye and were also identified as vestibular nuclear units. A further twelve units which responded to eye-movement could not be assigned to VN; the remaining 32 units were in VN but did not respond to passive eye-movement. Also, of 16 units whose recording sites were identified histologically in the VN complex, 11 gave responses to vestibular nerve stimulation and to passive eye-movement and 5 responded to eye-movement only.Control experiments eliminated auditory, visual and cutaneous sources for the signal produced by passive eye-movement; thus, the signal must have arisen from intraorbital proprioceptors. Units in VN were also found which were excited by electrical stimulation of the intraorbital part of the fourth (trochlear) nerve; this provides strong evidence that proprioceptors in the extrinsic ocular muscles (EOM) are included in the receptors which provide the signal to VN during passive eye-movement.The effects of vestibular stimulation and of passive eye-movement were found to interact upon units in VN. When passive eye-movement and vestibular stimulation were paired the response to the second stimulus was significantly reduced over a range of interstimulus intervals.The conclusions are that orbital proprioceptive signals, including those from the EOM, project to the vestibular nuclei in the toad and, there, are able to influence processing of vestibular afferent signals. We suggest, therefore, that orbital proprioceptive signals may play a part in oculomotor control. The significance of the results is discussed in relation to the strategic position of the VN in the oculomotor control system.     

The time course of the tonic oculomotor proprioceptive signal in area 3a of somatosensory cortex

A proprioceptive representation of eye position exists in area 3a of primate somatosensory cortex (Wang X, Zhang M, Cohen IS, Goldberg ME. Nat Neurosci 10: 640-646, 2007). This eye position signal is consistent with a fusimotor response (Taylor A, Durbaba R, Ellaway PH, Rawlinson S. J Physiol 571: 711-723, 2006) and has two components during a visually guided saccade task: a short-latency phasic response followed by a tonic response. While the early phasic response can be excitatory or inhibitory, it does not accurately reflect the eye's orbital position. The late tonic response appears to carry the proprioceptive eye position signal, but it is not clear when this component emerges and whether the onset of this signal is reliable. To test the temporal dynamics of the tonic proprioceptive signal, we used an oculomotor smooth pursuit task in which saccadic eye movements and phasic proprioceptive responses are suppressed. Our results show that the tonic proprioceptive eye position signal consistently lags the actual eye position in the orbit by ~60 ms under a variety of eye movement conditions. To confirm the proprioceptive nature of this signal, we also studied the responses of neurons in a vestibuloocular reflex (VOR) task in which the direction of gaze was held constant; response profiles and delay times were similar in this task, suggesting that this signal does not represent angle of gaze and does not receive visual or vestibular inputs. The length of the delay suggests that the proprioceptive eye position signal is unlikely to be used for online visual processing for action, although it could be used to calibrate an efference copy signal.     

Afferent signals from cat extraocular muscles in the medial vestibular nucleus, the nucleus praepositus hypoglossi and adjacent brainstem structures

The responses of single units in the vestibular nuclei, nucleus praepositus hypoglossi and in the brainstem, deep and posterior to the abducens nucleus, were studied in anaesthetized, paralysed cats. Natural vestibular stimulation was provided by horizontal, sinusoidal oscillation of the animal and extraocular muscle afferents of the ipsilateral eye were activated either by passive eye-movement or by electrical stimulation of the inferior oblique branch of the oculomotor nerve in the orbit. Unit responses to vestibular and/or orbital stimuli were examined in sets of peristimulus time histograms interleaved in time. Of 127 units exposed to both types of stimulus, 40 (32%) responded only to vestibular input; 46 (32%) were affected only by the orbital afferent signal and 19 (15%) received both signals; the remaining 22 units (17%) were discarded because they had polymodal (usually somaesthetic) input. Of the 93 units whose recording sites were determined histologically, 24 were in the medial vestibular nucleus, 16 in the n. praepositus hypoglossi and 45 in the magnocellular nucleus of the reticular formation posterior and deep to the abducens nucleus. In these three nuclei 19 units in total were found which carried the orbital proprioceptive afferent signal and also responded to horizontal vestibular stimulation. The input from the eye muscles proved able to modify the vestibular response by adding excitation or inhibition or both. Effects of the orbital signal were generally phasic. About half of the units which responded to passive eye-movement showed statistically significant differences between their responses to horizontal and to vertical eye-movement. We have shown previously that signals from extraocular muscle proprioceptors reach the vestibulo-oculomotor system in an amphibian and a bony fish; the present experiments show that this is the case in a mammal also. The fact that the visual and visuomotor behaviour of these three species is very different suggests that the proprioceptive signal may play some rather fundamental role in the vestibulo-ocular system. The principal interest of the present results is that they demonstrate that units in the central vestibular system of the cat, in structures which are known to be concerned in oculomotor control, and particularly in the organization of horizontal eye-movement, receive an afferent signal from the eye muscles during passive eye-movement. These brainstem nuclei are known to receive various combinations of input from the vestibular and visual systems and of signals which represent neck movement and eye position and 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.     

The proprioceptive representation of eye position in monkey primary somatosensory cortex

The cerebral cortex must have access to an eye position signal, as humans can report passive changes in eye position in total darkness, and visual responses in many cortical areas are modulated by eye position. The source of this signal is unknown. Here we demonstrate a representation of eye position in monkey primary somatosensory cortex, in the representation of the trigeminal nerve, near cells with a tactile representation of the contralateral brow. The neurons have eye position signals that increase monotonically with increasing orbital eccentricity from near the center of gaze, with directionally selectivity tuned in a Gaussian manner. All directions of eye position are represented in a single hemisphere. The signal is proprioceptive, because it can be obliterated by anesthetizing the contralateral orbit. It is not related to foveal or peripheral visual stimulation, and it represents the position of the eye in the head and not the angle of gaze in space.     

Single unit receptive fields in rabbit primary binocular cortex

Summary The receptive fields of 125 single units recorded from the binocular region of rabbit primary visual cortex have been analysed. The population of 43% radially symmetric, 23% directional, and 23% orientation selective units is similar to that of rabbit monocular visual cortex. The relative scarcity of orientation selective units and the absence of orientation columns differentiates rabbit from cat primary visual cortex. However, the majority of binocular units had similar receptive fields in each eye and very unconventional receptive fields were not encountered. Tested binocular units demonstrated summation upon simultaneous stimulation of both receptive fields. In conjunction with findings reported elsewhere, these results suggest that rabbit and cat possess a similar provision for binocular vision in spite of some differences in their cortical organisation.     

Visual motion processing for the initiation of smooth-pursuit eye movements in humans

We have used the initiation of pursuit eye movements as a tool to reveal properties of motion processing in the neural pathways that provide inputs to the human pursuit system. Horizontal and vertical eye position were recorded with a magnetic search coil in six normal adults. Stimuli were provided by individual trials of ramp target motion. Analysis was restricted to the first 100 ms of eye movement, which precedes the onset of corrective feedback. By recording the transient response to target motion at speeds the pursuit motor system can achieve, we investigated the visual properties of images that initiate pursuit. We have found effects of varying the retinal location, the direction, the velocity, the intensity, and the size of the stimulus. Eye acceleration in the first 100 ms of pursuit depended on both the direction of target motion and the initial position of the moving target. For horizontal target motion, eye acceleration was highest if the stimulus was close to the center of the visual field and moved toward the vertical meridian. For vertical target motion, eye acceleration was highest when the stimulus moved upward or downward within the lower visual field. The shape of the relationship between eye acceleration and initial target position was similar for target velocities ranging from 1.0 to 45 degrees/s. The initiation of pursuit showed two components that had different visual properties and were expressed early and late in the first 100 ms of pursuit. In the first 20 ms, instantaneous eye acceleration was in the direction of target motion but did not depend on other visual properties of the stimulus. At later times (e.g., 80-100 ms after pursuit initiation), instantaneous eye acceleration was strongly dependent on each property we tested. Targets that started close to and moved toward the position of fixation evoked the highest eye accelerations. For high-intensity targets, eye acceleration increased steadily as target velocity increased. For low-intensity targets, eye acceleration was selective for target velocities of 30-45 degrees/s. The properties of pursuit initiation in humans, including the differences between the early and late components, are remarkably similar to those reported by Lisberger and Westbrook (12) in monkeys. Our data provide evidence that the cell populations responsible for motion processing are similar in humans and monkeys and imply that the functional organization of the visual cortex is similar in the two species.     

The primary visual cortex in the mouse: Receptive field properties and functional organization

Summary Receptive field (RF) characteristics of cells in primary visual cortex of the mouse (C57B16 strain) were studied by single unit recording. We have studied the functional organization of area 17 along both the radial and tangential dimensions of the cortex. Eighty seven percent of the visual neurons could be classified according to their responses to oriented stimuli and to moving stimuli. Cells which preferred a flashed or moving bar of a particular orientation and responded less well to bars of other orientations or to spots, were classified as orientation selective (simple RF 23%, complex RF 18%). The majority of them were, moreover, unidirectional (24%). All orientations were roughly equally represented. Cells with oriented RFs were recorded mostly in the upper part of cortical layers II–III, where they appeared to be clustered according to their preferred orientation. Neurons that responded equally well to spots and bars of all orientations (46%) were classified as non-oriented; among these neurons there were several subcategories. Cells which responded equally well to spots and bars but preferred stimuli moving along one or both directions of a particular axis were classified as non oriented asymmetric cells (unidirectional 14%, bidirectional 4%). They were recorded mainly in supra- and infra-granular layers. Cells unaffected by stimulus shape and orientation which responded equally well to all directions of movement were classified as symmetric units. They had receptive field classified as ON (11%), OFF (1%), ON/ OFF (11%), or were unresponsive to stationary stimuli (5%). These cells were mostly found in layer IV, in which they constituted the majority of recorded cells. There was no apparent correlation between the functional type and size of RFs. However, the greatest proportion of small RFs was found in layer IV. In the binocular segment of the mouse striate cortex, the influence of the contralateral eye predominated. Ninety five percent of cells in this segment were driven through the contralateral eye. However, 70% of cells were binocularly activated, showing that considerable binocular integration occured in this cortical segment. Ocular dominance varied less along the radial than along the tangential dimension of the cortex.     

Eye movement-related activities in cells of the lateral suprasylvian cortex of the cat

Investigation of eye movement-related activities and photic responsiveness using behaving cats demonstrated distinctive representations of eye movement signals in different areas of the lateral suprasylvian cortex: visual reafference in the medial bank of the middle suprasylvian sulcus and non-visual signals (proprioceptive reafference or efference copy) in the lateral bank.     

Discharge patterns of neurons in the pretectal nucleus of the optic tract (NOT) in the behaving primate

1. To determine the possible role of the primate pretectal nucleus of the optic tract (NOT) in the generation of optokinetic and smooth-pursuit eye movements, we recorded the activity of 155 single units in four behaving rhesus macaques. The monkeys were trained to fixate a stationary target spot during visual testing and to track a small moving spot in a variety of visual environments. 2. The majority (82%) of NOT neurons responded only to visual stimuli. Most units responded vigorously for large-field (70 x 50 degrees) moving visual stimuli and responded less, if at all, during smooth-pursuit eye movements in the dark; many of these units had large receptive fields (greater than 10 x 10 degrees) that included the fovea. The remaining visual units responded more vigorously during smooth-pursuit eye movements in the dark than during movement of large-field visual stimuli; all but one had small receptive fields (less than 10 x 10 degrees) that included the fovea. For all visual units that responded during smooth pursuit, extinction of the small moving target so briefly that pursuit continued caused the firing rates to drop to resting levels, confirming that the discharge was due to visual stimulation of receptive fields with foveal and perifoveal movement sensitivity and not to smooth-pursuit eye movements per se. 3. Eighteen percent of all NOT units ceased their tonic discharge in association with all saccades including the quick phases accompanying optokinetic or vestibular nystagmus. The pause in firing began after saccade onset, was unrelated to saccade duration, and occurred even in complete darkness. 4. Most (90%) of the visual NOT units were direction selective. They exhibited an increase in firing above resting during horizontal (ipsilateral) background movement and/or during smooth pursuit of a moving spot and a decrease in firing during contralateral movement. 5. The firing rates of NOT units were highly dependent on stimulus velocity. All had velocity thresholds of less than 1 degree/s and exhibited a monotonic increase in firing rate with visual stimulus velocity over part (n = 90%) or all (n = 10%) of the tested range (i.e., 1-200 degrees/s). Most NOT units exhibited velocity tuning with an average preferred velocity of 64 degrees/s.(ABSTRACT TRUNCATED AT 400 WORDS)     

Neuronal responses to eye muscle stretch in cerebellar lobule VI of the cat

Summary Extraocular proprioceptive input to cerebellar vermis, lobule VI, was investigated in cats under N₂O analgesia by recording neuronal responses to eye muscle stretch. Both optic tracts were transected and the periorbital skin and conjunctiva were locally anaesthetized. Eye rotation within the physiological range was achieved by applying a pull of predetermined length and tension to each of the eight musculi recti at their insertion to the globe. Within lobule VI, only small patches of cortex receive stretch receptor afferents. The information made available by these afferents corresponds to a change of eye position. Minimal responses were dependent upon angular deflections of a few degrees. Maximal response amplitudes were obtained within the physiological range of angular deflections and angular velocities for the units tested. Most cells responded to stretch of more than one muscle. Three types of convergence were found: (1) neurons responding according to a certain direction of a conjugated movement of both eyes, (2) neurons responding to movements in either direction of one plane, (3) more complicated response patterns.     

Neuronal responses in the visual cortex of awake cats to stationary and moving targets

Summary Over 300 single units from the visual cortex (within and around the projection of the central area) were recorded from awake and non-paralyzed cats (chronic preparation). Spontaneous activity of 25% of the neurons was below 3/sec, that of 75% above 3/sec (mean 7.65 spikes/sec). Diffuse illumination had only little influence, but nearly all neurons responded to stimulation with some sort of visual contrast. This would be either an irregularly moved shadow on the screen with irregular boundaries (e. g. a hand with moving fingers), a dark stripe moving in a certain direction, stationary parallel gratings with a certain orientation, or saccadic eye movements across a checkerboard. Although some neurons responding to one stimulus type could also be responsive to other stimuli, the majority of units only responded to one stimulus type. The responses to stationary gratings (alternating parallel dark and bright stripes) and to moving dark stripes are described in detail. Responses to stationary gratings showed no adaptation. The orientation of the grating stripes was critical for each neuron, the optimal and minimal response orientation were separated by about 90°. For movement sensitive neurons, the direction of the movement was critical. Most neurons had only one, some had two preferred directions separated by 180°. No statistically significant predominance of certain orientation or direction preferences was found. The preferred target velocity of movement sensitive neurons was between 10 and 60°/sec, above 80–100°/sec only occasional or no responses could be elicited. Neurons which responded to saccadic eye movements (above 300°/sec) in the presence of a checker board, usually did not respond to slower target movements below 100°/sec.The results support the view that the visual system has different channels for the perception of moving and of stationary objects.This work was supported by the Deutsche Forschungsgemeinschaft as a research project in the Sonderforschungsbereich Kybernetik (SFB 31).Dr. R.B. Freeman, jr., was supported by NIH-grant 363-93600-21, MF-428-69 during the period of this research.     

Target selection for saccadic eye movements: direction-selective visual responses in the superior colliculus.

We investigated the role of the superior colliculus (SC) in saccade target selection in rhesus monkeys who were trained to perform a direction-discrimination task. In this task, the monkey discriminated between opposed directions of visual motion and indicated its judgment by making a saccadic eye movement to one of two visual targets that were spatially aligned with the two possible directions of motion in the display. Thus the neural circuits that implement target selection in this task are likely to receive directionally selective visual inputs and be closely linked to the saccadic system. We therefore studied prelude neurons in the intermediate and deep layers of the SC that can discharge up to several seconds before an impending saccade, indicating a relatively high-level role in saccade planning. We used the direction-discrimination task to identify neurons whose prelude activity "predicted" the impending perceptual report several seconds before the animal actually executed the operant eye movement; these "choice predicting" cells comprised approximately 30% of the neurons we encountered in the intermediate and deep layers of the SC. Surprisingly, about half of these prelude cells yielded direction-selective responses to our motion stimulus during a passive fixation task. In general, these neurons responded to motion stimuli in many locations around the visual field including the center of gaze where the visual discriminanda were positioned during the direction-discrimination task. Preferred directions generally pointed toward the location of the movement field of the SC neuron in accordance with the sensorimotor demands of the discrimination task. Control experiments indicate that the directional responses do not simply reflect covertly planned saccades. Our results indicate that a small population of SC prelude neurons exhibits properties appropriate for linking stimulus cues to saccade target selection in the context of a visual discrimination task.     

Development of the kitten visual cortex depends on the relationship between the plane of eye movements and visual inputs

Summary 1. Previous experiments have demonstrated that eye movements, acting through the extraocular muscle (EOM) proprioceptive afferents, are necessary for the development of orientation selectivity in the cells of the kitten visual cortex. New experiments were carried out to study the effect of the plane of eye movements on the preferred orientation acquired by the visual cortical cells. 2. Darkreared (DR) kittens were operated on at 5–6 weeks of age. In the first series of experiments, 4 out of the 6 EOMs were removed bilaterally in such a way that both eyes could only move in a single plane, either vertical or horizontal. In the second series of experiments, the same operation was performed on one eye which was also sutured shut and, on the other side, the EOM were deafferented by intracranial section of the ophthalmic branch of Vth nerve and the eye left open. 3. 1–4 days after surgery the kittens were given 6 h of visual experience and 12 h later were prepared for visual cell recording in Area 17. 4. In kittens of the first series: orientation selectivity developed in the majority (60–65%) of visual cells, most of which encoded horizontal orientations when the eyes had moved in the vertical plane and vertical orientations when the eyes had moved in the horizontal plane. These results show that the plane of eye movements during early visual experience influences the distribution of preferred orientations with an orthogonal relation. Ocular dominance histograms were strabismic like. 5. In kittens of the second series: orientation selectivity developed in 40–50% of cells, about half of which were tuned for the orientation orthogonal to the direction of movement of the occluded eye, as in experiment I. The seeing, deafferented eye, presumably would have sent normal visual inputs centrally, corresponding to displacements on the retina in every direction since the ocular motility of that eye had not been disturbed. However, proprioceptive information about its movements was suppressed. As only some of the EOMs of the occluded eye were still present and connected, the conclusion is that the observed influence of the plane of eye movements acts through the proprioceptive afferents. The ocular dominance histograms showed: 1) a powerful change in favour of the seeing eye after only 6 h of monocular visual experience; 2) a larger effect of monocular visual experience in the hemisphere contralateral to the seeing eye; 3) a linkage between acquisition of orientation selectivity and shift in ocular dominance. 6. Our results suggest that normal development of orientation selectivity in visual cortical cells results from the close association of visual and EOM afferent inputs. It is suggested that these two signals must occur with a precise temporal relationship.     

Selection of visual targets activates prelunate cortical cells in trained rhesus monkey

Summary Cells in monkey prelunate association cortex display an enhanced visual activity after the onset of a stimulus in the receptive field, when the stimulus is simultaneously selected as a target for a saccadic eye movement. In the present study we observed a separate activation which is independent of the passive visual on-response and occurs in a given cell when the animal saccades to a steady stimulus in its receptive field. The activation begins when the stimulus is selected for foveation before the eye actually moves, but is not necessarily predictive for an eye movement.This work was supported by the Sonderforschungsbereich Hirnforschung und Sinnesphysiologie (SFB 70/Tp B7)     

Discharges of neurons in the dorsal paraflocculus of monkeys during eye movements and visual stimulation

Extracellular recordings were obtained from 319 input units and 304 Purkinje cells (P-cells) in the dorsal paraflocculus of alert monkeys trained to fixate a visual target. They changed discharge rates with either eye movement, eye position, or visual stimulus movement. Of the 319 input units, recorded in the granular layer or white matter, most were mossy fibers (MFs), but 90 (28%) showed characteristic cellular spikes. The latter units were probably granular cells (p-GC). Of the 319 input units, 163 (51%) showed bursts with saccades (burst units) and 62 (19%) showed a prelude on the average 124 ms prior to the onset of saccade (long-lead burst units). Sixty-five (20%) had tonic activity related to eye position and also showed bursts with saccades (burst-tonic units), and the remaining 29 (9%) showed only tonic activity (tonic units). MFs and p-GCs showed no significant differences in the proportion of each type of unit or in their response properties. The majority of burst units (63%) were pan directional, whereas all long-lead burst units had directional selectivity. The preferred directions of long-lead burst, burst tonic, and directionally selective burst units were found in all four quadrants. Position-related activity was found in 48% of the burst-tonic and tonic units to be linearly related to eye position and to show position threshold. The other units also had position thresholds but their activity was not monotonically related to fixation position. Six climbing fibers (CFs), 32 input units (including 13 p-GC), and 8 P-cells showed cyclic responses during sinusoidal movements of a visual pattern. One class of MF units (57%) responded only to the direction, whereas the others responded to both the direction and retinal-slip velocity. Both CF and P-cell units responded to sinusoidal retinal-slip velocity. Of 67 input units, 23 showed cyclic modulation in firing during sinusoidal eye movements in the horizontal plane. Nineteen were burst-tonic and four were tonic units. They also showed position sensitivity. The phase of the cyclic responses tended to lag behind the eye velocity during low-frequency trackings. Of 237 P-cells, 163 (68.8%) discharged with saccades (burst P-cells), 42 (17.7%) paused with saccades (pause P-cells), and 32 (13.5%) discharged with saccades in one direction and paused in the other (burst-pause P-cells). Position sensitivity was found in 38 P-cells; 12 were burst, 5 were pause, and 10 were burst-pause P-cells. Eleven did not respond with saccades.(ABSTRACT TRUNCATED AT 400 WORDS)     

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)     

Neck proprioceptive inputs to primate vestibular nucleus neurons

The contribution of neck proprioceptive signals to signal processing in the vestibular nucleus was studied by recording responses of secondary horizontal canal-related neurons to neck rotation in the squirrel monkey. Responses evoked by passive neck rotation while the head was held stationary in space were compared with responses evoked by passive whole body rotation and by forced rotation of the head on the trunk. Most neurons (76%; 45/59) were sensitive to neck rotation. The nature and strength of neck proprioceptive inputs varied and usually combined linearly with vestibular inputs. In most cases (94%), the direction of the neck proprioceptive input was "antagonistic" or "reciprocal" with respect to vestibular sensitivity and, consequently, reduced the vestibular response during head-on-trunk rotation. Different types of vestibular neurons received different types of proprioceptive input. Neurons whose firing behavior was related to eye position (position-vestibular-pause neurons and position-vestibular neurons) were often sensitive to the position of the head with respect to the trunk. The sensitivity to head position was usually in the same direction as the neuron's eye position sensitivity. Non-eye-movement related neurons and eye-head-velocity neurons exhibited the strongest sensitivity to passive neck rotation and had signals that were best related to neck velocity. The results suggest that neck proprioceptive inputs play an important role in shaping the output of the primate vestibular nucleus and its contribution to posture, gaze and perception.