1 Exp Brain Res (1990) 82: Experimental Brain Research 9 Springer-Vertag 1990 Saccade-related responses of centrifugal neurons projecting to the chicken retina G. Marin, J.C. Letelier, and J. Wallman Biology Department, City College, City University of New York, New York, NY 10031, USA Received September 18, 1989 / Accepted March 30, 1990 Summary. Centrifugal projections to several sensory systems modulate the afferent activity during active behaviors. To see whether such modulation occurred in the visual system, we recorded the activity of isthmo-optic neurons in awake chickens during eye movements. We find that the discharge of all isthmo-optic neurons tends to stop during saccades, although every neuron does not pause for every saccade. The pause begins at approximately the same time as the saccade, and pause duration is correlated with saccade duration. Pausing during saccades occurs in both dark and light suggesting that it is motoric rather that visual in origin. In addition, we find that the spontaneous activity of isthmo-optic neurons increases in darkness. We discuss the significance of the saccadic modulation of isthmo-optic activity in terms of possible functions of the centrifugal projection in modulation of ganglion cell activity. Key words: Isthmo-optic nucleus Saccades Retinal ganglion cells - Chickens Introduction Despite thirty years of study, the functions of the centrifugal projection to the avian retina are not well understood. Anatomical studies carried out in chickens and pigeons have demonstrated that the only source of centrifugal fibers to the birds' retina are the isthmo-optic nucleus (ION) of the caudal midbrain (McGill et al. 1966b; Cowan 1970) and the so-called ectopic cells surrounding the nucleus (Wolf-Oberhollenzer 1987). The ION receives a topographically organized projection from the ipsilateral optic tectum (McGill et al. 1966a). Neurons in the ION project back to the retinal quadrant that is the source of their visual input (McGill et al. 1966b). As a result of this anatomical arrangement, each part of the Offprint requests to. G. Marin (address see above) retina projects via the tectum to that part of the nucleus from which it receives its centrifugal afferents. The centrifugal fibers terminate in the inner plexiform layer of the retina, where they make large synapses on the primary processes of amacrine cells (Maturana and Frenk 1965; Dowling and Cowan 1966), and perhaps upon displaced ganglion cells (Maturana and Frenk 1965). Experiments in which the isthmo-optic tract was either electrically stimulated (Miles 1972c; Holden 1978) or reversibly cooled (Miles 1972d; Pearlman and Hughes 1976b) all show that the centrifugal activity enhances the response of retinal ganglion cells to visual stimulation. In chickens and pigeons this effect is produced mainly by centrifugal suppression of the ganglion cells' inhibitory surround (Miles 1972c; Holden 1978), presumably via amacrine cells. Despite these influences, only subtle visual deficiencies result from lesioning the ION or the isthtoo-optic tract (Rogers and Miles 1972; Shortess and Klose 1977; Knipling 1978). In other sensory systems, centrifugal fibers modulate the sensitivity of sensory cells during active movements of the animal. For example, the efferent fibers to the lateral line organs of fishes and amphibia fire during movements and prevent self excitation by inhibiting afferent discharge (Russell and Roberts 1974). On the other hand, efferents to the muscle spindles increase the responsiveness of the afferents while the muscle is shortening (Matthews 1982). The centrifugal fibers of the vestibular system in monkeys may function to extend the dynamic range of the afferents during large accelerations accompanying voluntary head movements (Goldberg and Fernandez 1980). To explore the possibility that the centrifugal activity in the visual system is also modulated by active movements, we recorded from ION neurons of awake chickens. We investigated the relation between the firing pattern of ION cells and eye movements. We found that ION cells, while discharging at a variable rate during fixational intervals, tend to pause during saccades. A preliminary report of these findings has been presented (Letelier et al. 1985).
2 264 Methods The experiments were carried out on 14 four-week-old White Leghorn chicks (Gallus gallus domesticus) hatched in the laboratory from eggs obtained from a commercial supplier. In each animal recordings were obtained from both IO nuclei in two sessions two or three days apart. To permit stabilizing the head during the experiment without obscuring vision, two days before the first recording session the animals were deeply anesthetized with Chloropent (0.35 ml per 100 g body weight), positioned in a stereotaxic apparatus, and an acrylic plate was attached with dental cement to the skull and to a pair of anchoring screws fixed to the frontal bones on each side of the head. Then, a bilateral craniotomy over both IONs was made without opening the underlying dura. A 4 x 8 mm acrylic chamber was cemented to the skull, filled with agar saline and sealed with low melting point wax. Animals recovered overnight and fed normally the following day. Eye movements were recorded using the magnetic field search coil technique. In most experiments only the horizontal component of eye movements was measured, but on some occasions the vertical or the torsional component was simultaneously measured by a second coil placed perpendicular to the first. On the day of the experiment the bird was anesthetized with halothane, and a search coil was attached to the eye contralateral to the side of the ION to be recorded from (for details of this method, see Wallman et al. 1982). After a recovery period of two hours, the animal was placed in an alternating magnetic field, the lower lid was retracted with a fine thread and the plastic chamber was opened, exposing the brain for electrode penetrations. The chamber was kept filled with saline solution. The animal, loosely wrapped in a towel, lay calmly throughout the experiment except for occasional episodes of vocalization and neck movement. Treatment of the animals was in accord with the Helsinki/APS agreement. Extracellular recordings were made using tungsten-in-glass microelectrodes (Merrill and Ainsworth 1972) with five to twenty Ixm of exposed tip. Microelectrodes were passed through the dura and advanced into the brain using an hydraulic micromanipulator. The recording system was conventional. Visual stimuli consisted of dark bars and squares moved on a tangent screen located about 50 cm from the bird's eye. Stimuli were moved by hand or reflected from a mirror mounted on a galvanometer driven by a sinusoidal or trapezoidal voltage function. Optokinetic stimulation was produced with a vertical striped drum that surrounded the animal, and was rotated at a constant velocity by a servo motor. For recordings in darkness, the animal was surrounded by black curtains and the room lights turned off. Single- or multi-unit activity from the IO nucleus together with the eye position signal were recorded on a FM tape recorder for subsequent analysis. In order to localize the recording sites, small lesions were produced by passing anodal current (usually 5 pa for 5 s) through the microelectrode. At the end of the first session, the birds were anesthetized with halothane, the incision over the eye sutured and the plastic chamber resealed. To reconstruct recording locations, the chicks were deeply anesthetized with pentobarbital and perfused ir~tracardially with 0.85% saline followed by 10% formalin. Brains were cut in 40 gm sections on a freezing microtome and stained with cresyl violet for histological analysis. Spike data and eye position were sampled by a DEC 11/73 computer at 1000 samples/s for 600 ms around each saccade, thereby sampling the unit activity at least 200 ms before and 200 ms after the saccade. These data were used to make peri-stimulus histograms synchronized with the beginning and the end of each saccade using one of two methods. The first method electronically detected the saccade beginning and end using a special purpose device that relied on the characteristic 25 Hz oscillation of the eye during saccades. This method had an uncertainity of +/- 5 ms for the beginning, and +/- 15 ms for the end of the saccades. To confirm our results, in a subset of the units the eye position and spike train were digitized, displayed on an oscilloscope, and the beginning and end of each saccade was marked by the user (uncertainty = +/- 1 ms). To express the rate of firing before, during and after saccades, we counted spikes during 100 ms intervals beginning 150 ms before saccade onset, at saccade onset, and at saccade offset, respectively. Results Fifty-one single-unit and multi-unit recordings were obtained from the ION. Twenty-two well resolved single- Unit and nine multi-unit recordings were used for quantitative analysis. Histological reconstruction of electrode penetrations showed that all the recordings were located within the ION (Fig. 1). In general, spikes were biphasic, with a positive-negative shape and durations longer than 700 gsec, as commonly recorded near cell bodies. These facts, along with the fact that all the cells except two presented clear visual responses, make us confident that our data are not significantly contaminated with recordings either from terminals in the nucleus or fibers passing through it. Visual responses To the extent that we could assess, given the presence of the frequent spontaneous eye movements, the cells showed most of the visual response properties previously reported in paralyzed decerebrate chicks (Miles 1972b): cells produced a weak or phasic discharge at the "on" and "off" of light, they responded more vigorously to movements of targets within the receptive fields (Fig. 2, top), and rapid movements were better stimuli than slower ones. Receptive fields were relatively small, with an average diameter of approximately 10 deg. Some units showed habituation to repetitive stimulation, but this was neither so strong nor so frequent a characteristic as reported by Miles in paralyzed decerebrate chicks. A dark square, 10 deg in size, quickly moved across the receptive field, produced a strong response and was used as a search stimulus as we advanced the electrode. Fig. 1. Photomicrograph of a transverse section through the isthmooptic nucleus, stained with cresyl violet, showing a marking lesion (arrow) made 200 lain below the region in which visually responsive neurons were encountered. Abbreviations: ION isthmo-optic nucleus; TeO rectum opticum; Ce cerebellum; Ipc nucleus isthmi, pars magnocellularis. Calibration bar= 500 gm
3 265 Fig. 2A-D. Isthmo-optic cell activity in relation to visual stimulation and saccades. A Visual response to a dark square, 8 degrees of side, moved sinusoidally up and down (peak velocity, 140 deg/s) through its receptive field. Arrows indicate the direction of the movement. Lower trace shows the position of the stimulus. B Activity of the same cell, recorded in darkness, in relation to spon- taneous saccades. Upper trace, horizontal position of the contralateral eye. (In birds, saccades have a prominent 25 Hz oscillation and a duration of 100 to 300 ms). The unit has a variable discharge rate during fixational intervals and pauses during saccades. C, D Activity of a different ION unit recorded in light. Note pausing during saccades In addition to showing responses to our visual stimuli, ION cells showed very irregular activity as the bird looked around the laboratory, with short periods of silence and bursting periods of spikes/second. Some of this irregular activity was probably due to eye- movement-related visual stimulation; in particular the bursting periods resembled the responses elicited by objects moved in the visual field. However, ION cells also discharged in darkness, even at a higher average rate. To assess the average discharge rate, we counted spikes
4 266 during periods of two to three minutes under light and dark conditions. To avoid contamination by saccades we averaged the number of spikes in periods of 100 ms beginning 150 ms before saccade onset. The discharge frequency for a sample of 9 units recorded in darkness was significantly higher (14.3 spikes/s) than of 11 units recorded in light (7.50 spikes/s) (Mann-Whitney U test, p=0.03). Oculomotor responses The most striking characteristic observed in ION cells recorded was that the activity in every unit tended to pause during saccades (Fig. 2), and during quick phases of optokinetic nystagmus. This was especially evident in more active cells, but could be seen in all cells by using peristimulus time histograms. The pauses cannot be explained merely in terms of an interruption of the visual input during saccades, because they also were observed in total darkness. Figure 3 shows raster displays representing the discharge of a cell, recorded both in light and in darkness, in relation to saccades. Because these data include saccades with different durations, raster displays are aligned both with the beginning of the saccades (left side of the figure) and with the end of saccades (right side of the figure). The histograms at the bottom show the activity displayed in the rasters above in bins of 4 ms. In light (Fig. 3A), the discharge of this cell decreased or paused near the onset of the saccades, the discharge was reduced or absent throughout the duration of the saccades and was resumed between 20 ms before and 20 ms after saccade completion. In complete darkness, the cell showed pauses in activity during saccades similar to those recorded in light (Fig. 3B). Comparison of the histograms in light and dark shows that in light the cell has a lower spontaneous discharge rate and shows an overshoot in firing rate after saccade completion. All ION cells recorded in these experiments decreased or interrupted their firing during most saccades. In order to quantify the depth of modulation of the ION activity by saccadic eye movements, we used a "pause index", defined as the percent decrease in firing during saccades relative to the rate before saccades (Fig. 4 legend). Figure 4A shows the distribution of pause index measured in a sample of units in light and in darkness. The firing rate during saccades showed a median decrease across units of 67% (range: 20% to 100%) in light and 72% (range: 40% to 100%) in darkness. This substantial decrement in the activity of ION cells during saccades presumably produces a significant modulation of the sensitivity of retinal neurons in synchrony with eye movements. To further investigate whether visual factors such as the movement of the retinal image contribute to the pause, we compared the depth of modulation by saccades for units tested in both light and dark (Fig. 4B). The median decrease in firing tends to be slightly higher (Mann-Whitney U test p = 0.03) in darkness, suggesting that the pause is not related to vision. (sp/sec) (.:,i,i:,;: I..,,. ', :.(. '~.:.':.,1'., r.,.'.,,.~.,,.,...., '. :..,.~ :~,~,~,,,,,. LIGHT i.-j I. 9,,.h 4,11L,,.I[L I A (sp/sec) Time (msec) "* ',,,~..'..:',,] " ' 'l ''..,'..,. ;,,,, 9,,, 9 '.,,. '.., DARK :.. ii.'. :.""' '..' "..".~':i ',. '~',,',,,'"v,,. ", ~,~,~,.'..,, ~/.' _,._~. ij..._,,,ijd~ul.. i ,2,,:#,,,,,', Time (msee)....,,,,h_~, i_ ~,J i~.i,i Time (msec) Time (msec) 300 Fig. 3A, B. Discharge of a isthmo-optic neuron in relation to spontaneous saccadic eye movements. The unit was recorded while the animal was in light A and in darkness B. Rasters in the left side of A, B are aligned on the onset of saccades; those in the right side are aligned on the end of the saccades. The vertical line extending through the rasters indicates the event used to align the rasters. Each dot in the raster display represents a single action potential, and the cell discharge during consecutive spontaneous saccades are shown as successive lines on the raster. The histograms at the bottom of A, B show the sum of the above rasters in bins of 4 ms. Because consecutive saccades with different durations were sampled together, the histograms shown directly below the rasters in A, B represent the distribution of saccade durations, as indicated by the percentage of saccades (minimum 0%, maximum 100%) ongoing at the indicated time from the synchronizing event. Thus in A (light), all saccades lasted at least 70 ms and none lasted more than 250 ms
5 r..) 5 r~ 0 4 "r 3 2 z 1 g b" < O O ~ ~176 o ~ o 7 ~6 ~ 4 1 A PAUSE INDEX PAUSE INDEX < I i O,260 SACCADE DURATION (msec) Fig. 5. Relation between pause duration and saccade duration. Each symbol represents a different unit. Only pauses starting within 50 ms of the saccade beginning and lasting more than 75 ms were plotted (see text). The pause duration tends to be overestimated because of the bursty firing of the ION neurons, which includes frequent gaps in firing even between saccades. The line shown is the linear regression of pause duration on saccade duration o "~ o o ,.,,, O 100 [3 Pause index in light Fig. 4A, B. Depth of modulation by saccades of discharge of units in the isthmo-optic nucleus. The firing rates were obtained by counting the number of spikes during two 100 ms intervals, one beginning 150 ms before (B) and the other at the onset (D) of saccades respectively. The pause index (100 x [B-D]/B) represents the percent decrease in average firing during saccades relative to the average firing before saccades. A Distribution of pause index measured in light and in darkness for units recorded in one or both conditions. 21 single-unit (filled bars) and 8 multi-unit (hatched bars) recordings were included in these histograms. B Scatter plot of pause index measured in dark and light, for 11 single-unit (open symbols) and 5 multi-unit (filled symbols) recordings made under both conditions The low and irregular activity of ION cells made it difficult to measure the timing of the pauses with respect to the beginning and end of the saccades. However, from histograms like those of Fig. 3, we estimated that the pauses started between 25 ms before and 25 ms after the beginning of the saccades and ended between 35 ms before and 35 ms after the end of the saccades, the median being 0 ms in both cases. To ascertain whether the saccade determined the duration of the pause or simply triggered it, we assessed the relation between saccade duration and pause duration in 104 well-defined saccade-related pauses of 6 ION units. We measured the pause duration as the longest interspike interval greater than 75 ms that began within 50 ms of the saccade beginning. If the adjacent interspike interval was greater than 50 ms, we included it in the pause to prevent single spikes from causing underestimation of the pause duration. We excluded cases in which fewer than 5 spikes occurred within our 600 ms sampling interval. The results show a moderate effect of saccade duration on pause duration (Fig. 5), with a slope of 0.61 (pooled results; for separated units, mean = 0.63, s.e.m. = 0.08) and an intercept of 101 ms (r=0.44, p<0.001). Thus, saccades may trigger a pause of at least 100 ms, with the duration being loosely determined by the saccade duration. The burstiness of the ION discharges and the variability in depth of modulation prevent us from being definitive on this point. As mentioned above, the discharge rate showed a transient increase just after saccades in light but not in dark. To quantify this effect, the ratio between average frequency after and before saccades was measured in a sample of units. As shown in Fig. 6, after saccades in light, units fired a median of 2.3 times the rate before the saccades; in darkness the median of this ratio was 0.9 (difference of the medians was significant, Mann-Whitney U test p<0.001). This relative increase in the discharge rate at the end of saccades observed only in light may represent a wave of excitation coming from the retina, as the visual scene becomes stable after the saccades. This idea is supported by the fact that the increase in firing was usually a discrete burst, beginning ms after the saccade ended. Because, in birds, saccades are frequently associated with blinks of the nictitating membrane, this transient excitation may also reflect the
6 268 J b E Z u~ b E z 4 2 6] 4-2- O I AFTER DISCHARGE RATIO B DARK o ~ AFTER DISCHARGE RATIO Fig. 6A, B. Increase in the firing of ION units at the end of saccades when the bird is in light A but not in dark B. The after-discharge ratio is the ratio between the average firing after saccades and the average firing before saccades, measured at intervals of 100 ms starting 30 ms after the end of saccades and 150 ms before the beggining of saccades respectively. A value grater than one indicates more spikes after the saccade than before it. 21 single-unit (filled bars) and 9 multi-unit (hatched bars) were included in these histograms reappearance of the visual image. For the same reason, the pause in activity could be correlated with blinks rather than saccades. We found, however, that pauses regularly occurred during saccades that were not associated with blinks. Discussion The results presented in this study show that the centrifugal fibers in the chicken optic nerve discharge at reduced rates during saccadic eye movements. This pause in activity is "oculomotor, rather than visual, in origin because it occurs in dark as well as in light and because it generally begins as soon as the saccade does; if the pause were visual in origin a latency of ms (Miles 1972c) would be expected. Finally, the spontaneous activity (between saccades) of the isthmo-optic neurons is higher in dark than in light. Mechanism of saccadic pause Because anatomical studies have shown no prominent local circuits or intrinsic axon collaterals in the ION (Crossland 1979), the pause is probably produced by extranuclear afferents, either the activation of an inhibit- ory signal or the interruption of an excitatory one during saccades. The most likely source of the pause is the input (predominantly excitatory [Holden 1968]) coming from the optic tectum, which is the main source of afferents to the ION. Because in birds, as in mammals, the tectum plays a role in generating spatially oriented eye and head movements (du Lac and Knudsen 1986; Wise et al. 1986), saccade-related signals may be carried by the tectal afferents to the ION. The tectal neurons that project to the ION have been anatomically identified, corresponding to a single layer of cells in the stratum griseum et fibrosum superficialis near the junction of sublaminae h and i (Crossland and Hughes 1978). In the chicken and the quail, their dendritic arbors have long ramifying branches oriented toward deeper layers (Uchiyama and Watanabe 1985; Marin et al. 1988) and shorter branches extending upward, toward lamina g. (In the pigeon, Woodson et al.  reported that dendrites extend to the superficial laminae where the fibers from the retina terminate.) Therefore, tecto-ion neurons might well integrate the input from the retina with oculomotor signals from deeper tectal layers. Another possibility is that the pause results from non-tectal inputs acting upon the ION. In an electron microscopy study, Crossland (1979) has shown that a distinct class of synaptic endings in the ION, constituting more than 30% of the total, remains after removal of the optic tectum. Earlier studies have suggested that afferents may come from the motor nuclei of the extraocular muscles (Huber and Crosby 1929; Agnaut and Reperant 1978). More recent studies, using the HRP tracing technique, have not confirmed this projection (Uchiyama and Watanabe 1985; Marin et al. 1988). More likely sources of these afferents are the contralateral ION, the hyperstriatum accessorium and the nucleus raphe (Woodson et al. 1989). Effect of saccadic pause As mentioned above, the centrifugal system modulates the sensitivity of retinal ganglion cells: electrical stimulation of the isthmo-optic tract increases the responsiveness of retinal ganglion cells to visual stimuli, while cooling it has the opposite effect. Activation of the centrifugal pathway reduces the effectiveness of the inhibitory surround of the ganglion cell receptive fields, and, in some cases, can directly increase the sensitivity of the center (Miles 1972c). The decreased activity of isthmooptic cells during saccades probably induces a decrease in the sensitivity of retinal ganglion cells during that period, just as the cooling of the IO tract has been shown to do. In mammals, a decrease in the transmission of visual information through the geniculo-striate system during saccades has been reported by some workers (Bartlett et al. 1976; Duffy and Burchfiel 1975) but not by others (Buettner and Fuchs 1973; Adey and Noda 1973). In humans, a decrease in visual sensitivity during saccades-saccadic suppression-has been shown psychophysically (Stevenson et al. 1986). Our results suggest that, during saccades, the centrifugal system of birds may
7 269 reduce visual sensitivity at the level of the retina, as suggested by Holden (1966). It may, however, be an oversimplification to describe the action of the centrifugal fibers as retinal saccadic suppression, in view of the evidence suggesting that the centrifugal activity specifically affects the potency of the inhibitory surround of the retinal ganglion cells (Miles 1972c), thereby altering their transfer function. Two types of alterations are plausible: In classical cat or monkey retinal ganglion cells with a concentric centersurround organization, the inhibitory effect of the surround confers contrast sensitivity, but the stronger influence of the center means that the neuron is also sensitive to the overall luminance of its receptive field. In such a neuron, lower centrifugal activity during saccades would increase the influence of the surround, shifting the neuron to being more contrast sensitive and less luminance sensitive. Alternatively, in motion-sensitive ganglion cells, commonly found in the avian retina (Miles 1972a; Pearlman and Hughes 1976a), interactions among receptive-field subunits may confer directional selectivity if activity at one location is delayed and multiplied by that at another, with inhibition among subunits (Reichardt 1987). Analogous to the case just discussed, centrifugal activity might alter the balance between motion- and luminance-selectivity, although electrophysiological studies of retinal ganglion cells have failed to show an effect of ION activity on motion sensitivity (Miles 1972c; Pearlman and Hughes 1976b). In summary, it is possible that decreased centrifugal activity during saccades may make retinal ganglion cells less sensitive but more selective. Function of centrifugal fibers Despite the strong influence that saccades have on the activity of the neurons projecting to the retina, we are not inclined to view the principal function of this projection as being simply saccadic modulation of retinal output, because the anatomical and physiological properties seem too elaborate for so simple a function. First, there is the two-fold retinotopy, whereby individual ION neurons project to the same retinal region from which they receive their visual afference. Second, although we found that the majority of the ION units consistently paused for most saccades, which is compatible with a global modulation mechanism acting upon the entire retina, the activity between saccades was very irregular, and multi-unit recordings showed that the activity of nearby cells was not tightly correlated. Therefore the modulation of retinal ganglion cells between saccades is presumably constantly changing. We speculate that the saccadic modulation of the isthmo-optic nucleus is one of several ways that centrifugal influences on the retinal ganglion cells are exerted. Others may be: (1) Monocular enhancement-in many birds the two eyes generally view rather different scenes. A differential activation of the two IONs might provide an attentional function by changing the relative activity sent to the brain by the two eyes. (A similar hypothesis was advanced by Holden 1966.) For example, a visual feature on the right side of the visual field might lead to a head movement to the right and a simultaneous enhancement of the responsiveness of the right eye. Part of the mechanism of this differential activation of the two IONs might be the mutual inhibiton between the two tecta (Robert and Cuenod 1969) or the commissural projection between the two IONs (Woodson et al. 1989). (2) Local enhancement-alternatively, the centrifugal projections might change the responsiveness of local retinal regions as the bird attends to different parts of the visual field (Holden 1966; Uchiyama 1989). This ability to enhance local retinal regions may be especially useful to birds like chickens, which have a relatively uniform ganglion cell spacing across the retina (Ehrlich 1981). (3) Peripheral enhancement-several lines of evidence suggest that ION activity might bias the visual system toward panoramic vision at the expense of focal or foveal vision. In ground-feeding avian species, which continually alternate between hunting for seeds and scanning for predators (Powell 1974), the ION is larger than in raptors (Shortess and Klose 1975; Weidner et al. 1987), and projects mostly to extrafoveate retina (Hayes and Holden 1983). ION-lesioned chicks are less responsive to moving peripheral targets while feeding (Rogers and Miles 1972). In addition, ION neurons adapt strongly to repetitive stimulation (Miles 1972b), a property appropiate to a warning function. Finally, ION neurons in chicks accumulate androgens (Meyer et al. 1976) and androgens cause chicks to perseverate at pecking (Andrew 1972); perhaps they do so by modulating ION function. (4) Dark-adaptation-The higher spontaneous ION activity observed in darkness presumably increases the size of receptive fields by suppressing the inhibitory surrounds (Miles 1972c; Pearlman and Hughes 1976b), similar to what has been observed in cat ganglion cells during dark adaptation (Barlow et al. 1957); this may increase the retinal sensitivity. Thus, the increase in ION activity in darkness may represent a centrifugal contribution to dark adaptation. This role for the centrifugal projection to the retina is well established in arthropods (Fleissner and Fleissner 1988). In conclusion, the decrease in firing of centrifugal neurons during saccades may be one example of the ways in which the ION modulates the sensitivity of retinal ganglion cells. This simple coupling between the centrifugal and the oculomotor systems may give insight into other more complex interactions, such as dynamic changes in visual attention coordinated with changes in gaze. Acknowledgements. We are grateful to F.A. Miles for reading this manuscript. This work was supported by NSF grant BNS and NEI grant 1 R15 EY References Adey WR, Noda H (1973) Influence of eye movements on geniculostriate excitability in the cat. J Physiol (Lond) 235: Agnaut P, Reperant J (1978) A light and electron microscopic study of the nucleus isthmo-optieus in the pigeon. Arch Anat Microsc Morphol 67:63-78 Andrew RJ (1972) Recognition processes and behavior, with special reference to effects of testosterone on persistence. In: Lehrman
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