Enhanced activation of neurons in prelunate cortex before visually guided saccades of trained rhesus monkeys

Summary Single unit recording from trained rhesus monkeys demonstrate that the activity of the prelunate cortex is enhanced when a visual stimulus becomes a target of saccadic eye movement. As a rule, the enhancement is spatially selective: it does not occur if the animal makes an eye movement away from, rather than towards the stimulus. The results show that the prelunate cortex has access to an extraretinal signal which is activated in association with events preceding visually guided eye movements. Whether the signal reflects the initiation of eye movement or the animal's interest in the stimulus, which he usually selects to initiate an eye movement, remains uncertain.Supported by the Deutsche Forschungsgemeinschaft (DFG), Sonderforschungsbereich Hirnforschung und Sinnesphysiologie (SFB 70, Tp. B7)     

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)     

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.     

Binocular interactions and disparity coding in area 21a of cat extrastriate visual cortex

We have examined, using both qualitative and quantitative techniques, binocular interactions of extracellularly recorded single neurons in the extrastriate cortical area 21a of anaesthetized and paralysed cats. Consistent with previous reports we have found that: (a) all area 21a neurons were orientation-selective, with about 65% of them preferring orientations within 30° of the vertical; and (b) over 75% of area 21a cells could be activated through either eye. Furthermore, a significant minority (4 cells; about 10%) of a subpopulation of 39 neurons in which binocular interactions were examined quantitatively, were obligatory binocular neurons, that is, they responded very weakly, if at all, to the monocular stimuli presented through either eye but responded vigorously to simultaneous stimulation through both eyes. Almost 70% (27/39) of neurons tested quantitatively for binocular interaction have shown significant modulation (over 50%) of their peak responses in relation to binocular positional retinal disparities. The majority of neurons sensitive to binocular positional disparities resembled either tuned excitatory (22 cells; 56.5% of the sample) or tuned inhibitory (2 cells; 5% of our sample) cells. In particular, they gave, respectively, maximal or minimal responses to optimally oriented, moving photic stimuli when the receptive fields plotted through each eye completely or partially overlapped. Although neurons recorded in area 21a have relatively large receptive fields (mean width 3.3±1.1°; range 2.0–5.6°), the mean width of the disparity tuning curve (2.8±1.0°; range 1.3–4.8°) for our sample of area 21a neurons was similar to those of neurons with significantly smaller receptive fields, recorded in areas 17 and 18 of cat's primary visual cortex. We conclude that area 21a of the cat, like areas 17 and 18 of primary visual cortex, is likely to play an important role in binocular depth discrimination and might constitute a higher order area for stereoscopic binocular vision.     

‘Real-motion’ cells in visual area V2 of behaving macaque monkeys

Summary Extracellular recordings were made in area V2 of behaving macaque monkeys. Neurons were classified into three groups: non-oriented cells, oriented cells with antagonistic areas and oriented cells without antagonistic areas in their receptive field. All neurons were tested with standard visual stimulations in order to assess whether they gave different responses to the movement of a stimulus and to the movement of its retinal image alone, when the stimulus was motionless and the animal voluntarily moved its eyes. To do this, 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 movements), were compared. 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. Out of a total of 263 neurons isolated in the central 10 deg representation of area V2, 101 were fully studied with the visual stimulation described above. Most of these (83/ 101; 82%) gave about the same response to the two situations. About 14% (14/101) gave a good response to stimulus movements during steady fixation and a very weak one to retinal image displacements of stationary stimuli during visual tracking. We have called neurons of this type real-motion cells (cf. Galletti et al. 1984). None of the non-oriented cells was a real-motion one, while about an equal percentage of real-motion cells was found among the oriented cells with and without antagonistic areas. Finally, we found only 4 neurons which showed behaviour opposite to that of real-motion cells, i.e. they showed a better response to displacement of the retinal image of stationary stimuli than to actual movement of stimuli. We suggest that real-motion cells might contribute to correctly evaluating movement in the visual field in spite of eye movements and that they might allow recognition of the movement of an object even if it moves across a non-patterned visual background. Present data on area V2, together with similar results observed in area V1 (Galletti et al. 1984; Battaglini et al. 1986), support the view that these two cortical areas analyse the movement in a parallel fashion along with many other characteristics of the visual stimulus.     

Retinal slip during active head motion and stimulus motion

Gaze control in various conditions is important, since retinal slip deteriorates the perception of 3-D shape of visual stimuli. Several studies have shown that visual perception of 3-D shape is better for actively moving observers than for passive observers watching a moving object. However, it is not clear to what extent the improved percept of 3-D shape for active observers has to be attributed to corollary discharges to higher visual centers or whether the improved percept might be due to improved gaze stabilization during active head movements. The aim of this study was to measure binocular eye movements and to make a quantitative comparison of retinal slip for subjects instructed to fixate a visual stimulus in an active condition (subject makes an active head movement, object is stationary) and in a passive condition (the stimulus moves, the subject is stationary) for various movement frequencies, viewing distances, and stimulus diameters. Retinal slip remains below the acuity threshold of about 4 deg/s in active conditions, except for the highest frequency tested in this study (1.5 Hz) for nearby targets (0.25 cm). Retinal slip exceeds this threshold for most passive conditions. These results suggest that the enhanced performance in the visual perception of 3-D shape during active head movements can, at least partly, be explained by better fixation by actively moving observers.     

Goal-directed vestibulo-ocular function in man: gaze stabilization by slow-phase and saccadic eye movements

Summary Vestibular function was examined during passive head movements having profiles that approximated the low-to-intermediate range of natural self-generated movements (10–220°/s peak velocity, about 0.5 s duration). A seated subject looked at a point target on the wall, the lights were extinguished and the chair was briefly turned while the subject tried to look at the just-viewed point. The chair was stopped, the lights were turned on again and the target was re-fixated, if necessary. Ocular stabilization was characterized (1) by net stabilization that was due to the combined effects of both slow-phase and rapid (saccadic or quick-phase) eye movements, (2) by cumulative-slow-phase stabilization that was due to slow-phase eye movements, and (3) by cumulative-saccadic stabilization that was due to effects of all rapid eye movements. It was found that both slow-phase and saccadic eye movements tended to keep the eyes on the actual unseen target. During repeatedly applied head movements, net and cumulative-slow-phase stabilization tended to be almost perfect. However, the average magnitude of the error in net stabilization (i.e., deviation from perfection) was always less than the corresponding error in slow-phase stabilization. This occurred because in a given turn, saccadic movements tended to supplement deficient slow-phase movements and to decrement excessive slow-phases. In 4 of 5 subjects, cumulative-saccadic stabilization tended to equal the error in cumulative-slow-phase stabilization. All results were unaffected by head velocities up to ±220°/s. It was concluded that these saccades tended to stabilize gaze (eye + head) in space during head movements in total darkness.     

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 position signals in human saccadic processing

Summary 1. We studied saccades to briefly flashed targets in 8 human subjects. The target flash occurred (i) during smooth pursuit (ramp-flash), (ii) just before a saccade to another target (step-flash), or (iii) during steady fixation (flash only). All lights were extinguished after the target flash so that smooth pursuit or saccadic eye movements occurred during the interval of complete darkness between the target flash and the saccade to it. We compared these saccades to those made without intervening eye movement (flash only), and quantified the extent to which the saccadic system compensated for the change in eye position that occurred during the dark interval. 2. Saccades to control flashes were reasonably accurate (mean gain 0.87) and consistent. Compensation for the intervening eye movement in the ramp-flash and step-flash paradigms was highly variable from trial to trial. On average, subjects compensated for 27% of the intervening pursuit eye movement on ramp-flash trials and for 58% of intervening saccadic movement on step-flash trials. 3. Multiple regression analysis showed that the variability did not depend on factors such as variations in underlying saccadic gain, response latency, timing of stimuli or size of the required response. We conclude that this variability is intrinsic to saccadic responses that require the use of an eye position signal. 4. These results show that an eye position signal is available to the saccadic system but that this signal has low fidelity. The high variability and low fidelity of the eye position signal suggest that the saccadic system does not normally operate in spatial coordinates, which require the use of an accurate eye position signal, but rather in retinal coordinates.     

A frontal cortical potential associated with saccades in humans

Summary We describe a frontal EEG potential which begins 25–35 ms before intentional saccadic eye movement. It consists of a 15–20 volt monophasic positive waveform with peak during or just after movement, and returns to EEG baseline 150–200 ms after its onset. The waveform is largest at a midline position just anterior to F_Z (10–20 system), is independent of visual input such as fixation guides, and is not related to saccade direction or amplitude. The potential is difficult to observe in some subjects and is independent of the pre-saccadic spike potential. It may be related to the discharge of single cortical neurons that signal the initiation of saccadic movements, but not their exact metrics; a possible generator is the supplementary eye fields of the dorsomedial prefrontal cortex.     

Saccade and blinking evoked by microstimulation of the posterior parietal association cortex of the monkey

Summary Electrical stimulation with microelectrodes of the posterior parietal association cortex in alert behaving monkeys elicited saccadic eye movements and blinking. The sites in which saccades were elicited by electrical stimulation were concentrated in the anteromedial part of area 7a, especially in the posterior bank of the intraparietal sulcus, in a region which sends efferent projections to the frontal eye field and the superior colliculus, but they were also found in the posterolateral part of area 7a. Compared with the frontal eye fields and the superior colliculus, the threshold current for eliciting saccades was relatively high, on the average 86 A. Moreover, the elicitation of saccade was inconsistent even with suprathreshold stimulation and suppressed during visual fixation. Latencies of the saccades were relatively long, on the average 50 ms; they were longer in the posterolateral part than in the anteromedial part. Direction and amplitude of evoked saccades depended on the site of stimulation, but was independent of eye position in most cases. However, goal-directed saccades which depended on initial eye position were elicited in three penetrations in the posterolateral part of area 7a. Blinking was elicited mainly in the lateral part of area 7a. The threshold of blinking was 70 A and the latency was 50 ms on the average. In contrast to saccades, blinking was elicited constantly with each stimulus even during attentive fixation. We occasionally recorded single unit activity at the site of stimulation with the same electrodes. More than half of the units recorded at the site of blinking responded to approaching visual stimulus. These results suggest that area 7a participates indirectly in the control of saccades by way of its connection to the frontal eye fields or the superior colliculus, and it may also play an important role in blinking in response to a visual threat.Prof. J. Hyvärinen died on February 26, 1983     

Firing characteristics of vestibular nuclei neurons in the alert monkey after bilateral vestibular neurectomy

Summary After destruction of the peripheral vestibular system which is not activated by moving large-field visual stimulation, not only labyrinthine-ocular reflexes but also optokinetic-ocular responses related to the velocity storage mechanism are abolished. In the normal monkey optokinetic-ocular responses are reflected in sustained activity changes of central vestibular neurons within the vestibular nuclei. To account for the loss of optokinetic responses after labyrinthectomy, inactivation of central vestibular neurons consequent on the loss of primary vestibular activity is assumed to be of major importance. To test this hypothesis we recorded the neural activity within the vestibular nuclear complex in two chronically prepared Rhesus monkeys during a period from one up to 9 and 12 months after both vestibular nerves had been cut. The discharge characteristics of 829 cells were studied in relation to eye fixation, and to a moving small and large (optokinetic) visual stimulus producing smooth pursuit (SP) eye movements and optokinetic nystagmus (OKN). Units were grouped into different subclasses.After chronic bilateral vestibular neurectomy (BVN) we have found: (1) a rich variety of spontaneously active cells within the vestibular nuclear complex, which — as far as comparison before and after BVN is possible — belong to all subclasses of neurons functionally defined in normal monkey; and (2) no sustained activity changes which are related to the activation of the velocity storage mechanism; this is especially true for pure-vestibular, vestibular-pause and tonic-vestibular-pause cells in normal monkey which show a pure, pause and tonic-pause firing pattern after BVN. Neurons which are modulated by eye position are, however, modulated with the velocity of slow eye movements with comparable sensitivity during SP and OKN. Retinal slip is extremely rarely encoded. The results of the present study do not directly answer the question why the velocity storage mechanism is abolished after BVN but they suggest that only a small number of central vestibular cells may be inactivated by neurectomy.Supported by SNF grant no. 3.510-0.86     

The gap effect and inhibition of return: interactive effects on eye movement latencies

Three experiments are reported with two types of manipulations that are known to affect the latency with which subjects can initiate saccadic eye movements. The first manipulation involves the temporal relation between the offset of a visual fixation point and the onset of a peripheral target (the gap effect). The second manipulation involves the prior allocation and removal of visual attention (inhibition of return). In two experiments, the gap effect was smaller for saccades to previously attended locations than to previously unattended locations. The results suggest an important link between the two phenomena and provide new insights into the brain mechanisms underlying visual attention and eye movements.     

Frontal lobe lesions in man cause difficulties in suppressing reflexive glances and in generating goal-directed saccades

Summary The frontal eye field (FEF) and superior colliculus (SC) are thought to form two parallel systems for generating saccadic eye movements. The SC is thought classically to mediate reflex-like orienting movements. Thus it can be hypothesized that the FEF exerts a higher level control on a visual grasp reflex. To test this hypothesis we have studied the saccades of patients who have had discrete unilateral removals of frontal lobe tissue for the relief of intractable epilepsy. The responses of these patients were compared to those of normal subjects and patients with unilateral temporal lobe removals. Two tasks were used. In the first task the subject was instructed to look in the direction of a visual cue that appeared unexpectedly 12° to the left or right of a central fixation point (FP), in order to identify a patterned target that appeared 200 ms or more later. In the second anti-saccade task the subject was required to look not at the location of the cue but in the opposite direction, an equal distance from FP where after 200 ms or more the patterned target appeared. Three major observations have emerged from the present study. (a) Most frontal patients, with lesions involving both the dorsolateral and mesial cortex had long term difficulties in suppressing disallowed glances to visual stimuli that suddenly appeared in peripheral vision. (b) In such patients, saccades that were eventually directed away from the cue and towards the target were nearly always triggered by the appearance of the target itself irrespective of whether or not the anti-saccade was preceded by a disallowed glance. Those eye movements away from the cue were only rarely generated spontaneously across the blank screen during the cue-target time interval. (c) The latency of these visually-triggered saccades was very short (80–140 ms) compared to that of the correct saccades (170–200 ms) to the cue when the cue and target were on the same side, thereby suggesting that the structures removed in these patients normally trigger saccades after considerable computations have already been performed. The results support the view that the frontal lobes, particularly the dorsolateral region which contains the FEF and possibly the supplementary motor area contribute to the generation of complex saccadic eye-movement behaviour. More specifically, they appear to aid in suppressing unwanted reflex-like oculomotor activity and in triggering the appropriate volitional movements when the goal for the movement is known but not yet visible.     

Retinotopic organization of extra-retinal saccade-related input to the visual cortex in the cat

Summary Single unit activity of 842 cells has been recorded in cat visual cortex and analyzed with respect to vestibular induced, and spontaneous saccadic eye movements performed in the dark. This study has been done in awake, chronically implanted cats, subsequently placed in acute conditions to achieve the precise retinotopic mapping of the cortical areas previously investigated.In areas 17 and 18, respectively, 27% and 24% of the cells tested were influenced by horizontal saccadic eye movements in the dark (E. M. cells). In the Clare-Bishop area, the proportion of E. M. cells was 12%, while only 2% of such cells were found in areas 19 and 21.The distribution of E.M. cells in areas 17 and 18 with respect to retinotopy showed that E.M. cells were more numerous in the cortical zones devoted to the representation of the area centralis (38% in area 17, 27% in area 18) than in the zones subserving the periphery of the visual field (17% and 12%, respectively).Two of the characteristics of E. M. cell activations appear dependant on the retinotopic organization. First, a larger number of E.M. cells presenting an asymmetry in their responses to horizontal saccadic eye movements in opposite directions (directional E.M. cells) were encountered in the cortical representation of the peripheral visual field. 53% of E. M. cells recorded in area 17 and 71% in area 18 were directional in the cortex corresponding to the peripheral visual field. This percentage was of 23% and 25% respectively in the cortex devoted to area centralis. Second, E.M. cells were found to have a latency from the onset of the saccade systematically larger than 100 ms (i.e, they discharged at, or after the end of the eye movement) if they were located in the cortical representation of the area centralis, while E.M. cells related to the peripheral visual field displayed a wider range of latencies (0–240 ms).Results obtained in Clare Bishop area, although limited to the representation of the peripheral visual field, were quantitatively and qualitatively similar to those observed in the homologous retinotopic zones of areas 17 and 18.It is concluded that an extra-retinal input related to oculomotor activity is sent to the cat visual cortex and is organized, at least in areas 17 and 18, with respect to the retinotopic representation of the visual field. These data support the hypothesis of a functional duality between central and peripheral vision and are discussed in the context of visual-oculomotor integration.Supported by INSERM (C.R.L. 79-53336)     

“Dumping” of rebound nystagmus and optokinetic afternystagmus in humans

Rebound nystagmus (RN) is an involuntary movement of the eyes, characterized by slow-phase eye velocity in the direction of previously maintained eccentric gaze. The purpose of this study was to clarify the neural or neuromuscular events that are responsible for the generation of RN. To do so, we examined whether a briefly presented visual stimulus during RN reduces (i.e., dumps) subsequent eye velocity, compared with the velocity of slow-phase eye movements when no visual stimulus was presented. For comparison, dumping was examined also for optokinetic afternystagmus (OKAN), which is generally believed to result from eye-velocity signals stored in a central neural integrator as a consequence of optokinetic stimulation. Results obtained from ten normal observers showed that RN and OKAN both exhibit dumping: average slow-phase eye velocities were reliably slower after fixation of a 0.6 deg stationary target than on trials when no fixation target was presented. Although RN decayed faster than OKAN in darkness, the magnitude of dumping increased similarly with the duration of the visual stimulus (25 ms to 4 s) for both types of eye movement. The results imply that signals from a central velocity-storage mechanism contribute to the generation of RN.     

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.     

Auditory cortex neurons sensitive to correlates of auditory motion: underlying mechanisms

Summary Neuronal response properties such as phasic vs. tonic, onset vs. offset, monotonicity vs. non-monotonicity, and E/E vs. E/I, can be shown to act synergistically suggesting underlying mechanisms for selectivity to binaural intensity correlates of auditory sound source motion. Both identical (diotic), and oppositely directed dichotic AM ramps were used as stimuli in the lightly anesthetized cat, simulating motion in four canonical directions in 3-dimensional space. Motion in either azimuthal direction evokes selective activity in cells which respond best to the onset of monaural sound in one ear and show a decreased response to binaural stimulation (E/I or I/E). In some cells specificity is increased by off components in the non-dominant ear. Although these cells fire only at the onset of stationary sound, they fire throughout oppositely directed AM ramps. Motion toward or away from the head evokes responses from EE cells; strong binaural facilitation increases selectivity for motion in depth. The sharpness of direction of tuning was related to the degree of binaural facilitation in E/E cells. Selectivity for sound moving away from the head is correlated with off responses, while on responses correlate with preference for motion toward the head. Most units showed a monotonic rate function as AM ramp excursion and rate was increased. One third were selective for slower rates of intensity change and may therefore encode slower rates of stimulus motion, as well as direction of movement. The findings suggest that neural processing of auditory motion involves neural mechanisms distinct from those involved in processing stationary sound location and that these mechanisms arise from interactions between the more traditionally studied response properties of auditory cortex neurons.This research was supported by MRC of Canada grant no MA-9856 to M.S.C., and a MRC studentship to E.S.     

Adaptive plasticity in the gaze stabilizing synergy of slow and saccadic eye movements

Summary When a normal human subject is briefly turned in total darkness while trying to look at a spatially fixed target, the vestibulo-ocular reflex (VOR) produces slow-phase compensatory eye movements tending to hold the eyes on target. However, slow-phase compensation per se is generally inadequate in these circumstances. Nevertheless it has recently been found, that even in the dark, this inadequacy tends to be corrected by supplementary saccades usually acting in the compensatory direction. The present study further investigates this phenomenon by measuring the respective contributions of saccadic, slow-phase and overall net compensation in 9 subjects tested before and after 30% adaptive attenuation of VOR slow-phase gain. In each test series, subjects attempted to stabilize their gaze on a previously seen target during each of 40 brief (0.5 s) whole body rotations (40°/s, 20° amp) conducted in complete darkness. The adaptive experience comprised 2 h of full-field visual suppression of the VOR during sinusoidal rotation of subject and surround at 1/6 Hz and 40°/s velocity amplitude. Before adaptation, the cumulative slow-phase and cumulative saccadic components produced on average 78% and 14% respectively of the ideal (100%) compensation, thus yielding an overall net compensation which was 92% of the desired value. After adaptation, the corresponding values in the same population were 53%, 18% and 71% respectively. Thus after adaptation, the combined saccadic-slow-phase response brought the final gaze position to a point in space that was systematically shifted in the direction of head rotation (i.e. undercompensation). Subjects re-exposed to 30 min of normal visual-vestibular interaction displayed a variety of recovery patterns using different combinations of slow and saccadic eye movements. However, there was a consistent synergistic tendency for saccadic eye movements to improve slow-phase performance, regardless of the subject's adaptive state. In one subject, compensatory saccadic eye movements corrected a consistent directional asymmetry in the slow-phase response. It is suggested that a conscious vestibular percept of self-rotation might underlie the combined saccadic-slow-phase response, and that the net under performance after adaptation might reflect attenuation of this percept relative to the actual rotational stimulus.     

Visual properties and spatial distribution of neurones in the visual association area on the prelunate gyrus of the awake monkey

Summary We have analysed, in the awake monkey (Macaca sylvana) the functional properties of 489 neurones in the prelunate visual area (PVA, largely corresponding to V4). PVA has a coarse retinotopic organization with the lower quadrant of the visual field represented along the prelunate gyrus. The visual periphery is located medio-dorsally, the central visual field laterally near (and within?) the inferior occipital sulcus and the upper quadrant latero-ventrally. The vertical meridian runs caudally within the lunate sulcus, the horizontal meridian crosses the prelunate gyrus and continues into the superior temporal sulcus. Receptive field diameters of neurones vary between 1° and 10° with increase towards the visual periphery, but are strictly confined to the contralateral visual field. 28% of the neurones showed spectral sensitivity. About half of these cells had strong spectral opponency, the other half showed only weak opponency with broader spectral response curves. 11 cells (2%) showed striking centre/surround interactions with inhibition, disinhibition or occlusion of the two mechanisms, and different spectral response ranges of the centre and the surround, respectively. 43% of the prelunate cells were responsive to various spatial features without spectral sensitivity. We distinguished on- and off-center cells (2%), direction and movement sensitive cells (10%) and cells sensitive to gratings of parallel lines within a limited range of orientations (about 10%). A special group were cells which responded strongly to stimuli which contained many contrasts (textures without specific orientations and without regular spatial arrangements) (9%). Many of these cells were specifically responsive to variations of the internal structure of such stimuli. 3% of the cells were strongly activated in connection with behaviour: 11 neurones discharged strongly when the monkey looked attentively at a human face or when he responded with facial expressions to a threatening expression of a person. Photographs of faces were not effective. Some neurones (1%) were activated in connection with eye movement. These neurones were found in the lateral part of the prelunate gyrus. Neurones with spectral or non-spectral properties were clustered within small, irregularly shaped patches of 1–4 mm diameter. It is concluded that the prelunate visual cortex, which we consider as part of area 19, is not just a colour area, but represents various features of the visual environment (including colour, luminance, movement, texture and behavioral significance), and relates them — through its subcortical and cortical outputs — to behaviour. The various visual cortical areas may be seen as a cooperative of several connections between visual input and behaviour output rather than as links in a hierarchical chain of perceptual and cognitive representations.