Exp. Brain Res. 25,487-509 (1976)

Experimental Brain Research 9 by Springer-Verlag1976

Influence of Saccadic Eye Movements on Geniculostriate Excitability in Normal Monkeys* J.R. Bartlett, R.W. Doty, Sr., B.B. Lee a and H. Sakakura 2 Center for Brain Research, Universityof Rochester, Rochester, New York 14642 (USA)

Summary. Using permanently implanted electrodes in squirrel monkeys and macaques, transmission through the lateral geniculate nucleus ( L G N ) was assayed from the amplitude of potentials evoked in optic radiation by an electrical pulse applied to optic tract. A v e r a g i n g of either individually or machine selected potentials, elicited at 0.3, 1.0, 20 or 50 Hz, in all cases showed a decrease in transmission ranging from 5 - 6 0 % in the period after saccadic eye m o v e m e n t s m a d e ad libitum. The suppression was greater in a patterned visual environment than in diffuse illumination, which in turn was greater than that occurring following saccades in the dark. Demonstration of the effect in darkness always required data averaging and never exceeded 20 %. The effect was consistently greater in the magnoceUular than parvocellular component. Suppression was often abruptly terminated and replaced by a facilitation of 5 - 1 5 % about 100 msec after saccade detection. C o m p a r a b l e effects were observed for excitability of striate cortex tested by a stimulus pulse applied to optic radiation. In addition, sharply demarcated potentials inherently arising in L G N and striate cortex were found in association with saccades m a d e even in total darkness. Neglecting a possible but dubious contribution from eye muscle proprioceptors, the experiments establish the existence of a centrally originating m o d u l a t i o n o f visual processing at both L G N and striate cortex in relation to saccadic eye m o v e ment in primates. This modulation m a y partially underlie the p h e n o m e n o n of "saccadic suppression" and hasten the acquisition of a meaningful visual sample immediately following an ocular saccade. It remains uncertain as to how it may relate to similar or greater effects accompanying changes in alertness, or to fluctuations of unknown origin occurring sometimes semirhythmically at 0.05-0.03 Hz (Fig. 7). Key words: Saccadic eye m o v e m e n t s - Visual system - "Corollary discharge" - Primates. * Supported by Grant NS 03606 and Contract 70-2279 from the National Institutes of Neurological Diseases and Stroke, National Institutes of Health and by Grant GB 7522X from the National Science Foundation. B. B. L. was also aided by a travel grant from the Wellcome Trust (U. K.) and H.S. received a travel grant from the International Brain Research Organization. 1 Present address: B.B.L.: Max-Planek-Institut fiir Biophysikalische Chemic, Karl-FriedrichBonhoeffer-Institut, G6ttingen-Nikolausberg, Federal Republic of Germany. 2 H.S.: Department of Psychiatry, Sumitomo Hospital, Osaka, Japan.

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It must be inferred from the rapid disappearance of stabilized retinal images (e.g., Yarbus, 1967; Sharpe, 1972) that movement of the eyes is normally essential to vision. If this be true, it may equally be expected that central visual processes have evolved in such a way that they are linked to ocular movements. Each saccadic eye movement (SEM) in most lighted environments inevitably generates a large signal from the retina consequent to the sudden transit of contrast patterns. This transient stimulus accompanying an SEM yields a negligible subjective effect, whereas comparable transients generated by abrupt movement of the visual field or manual displacement of the eye are readily perceived. This difference in the effect of self generated versus externally generated visual input provides prima facie evidence for a modification of visual processes in relation to SEMs. It is apparent that there are two, somewhat separable, facets to this modification, one related to reduced sensorial effect in relation to an SEM, the other concerning recognition of the causation of transient visual events. The first presumably involves the phenomenon of "saccadic suppression" (Matin, 1974) and the second concerns the more general problem of self-originated sensation as dealt with in the concepts of the "corollary discharge" (Sperry, 1950) or "Efferenzkopie" (von Hoist and Mittelstaedt, 1950). In a thorough and analytical review of these concepts MacKay (1973) has distinguished three potential sources for such modulation of visual input: 1. proprioceptive feedback from extraocular muscles; 2. the retinal signal itself; 3. a centrally controlled gating of the visual system concomitant with the excitation of the oculomotor saccadic system. There is no evidence that proprioception makes a significant contribution to the modulation, and rather decisive evidence that it does not (Brindley and Merton, 1960). On the other hand, MacKay (1973) and Mitrani et al. (1975) have shown that "saccadic suppression" occurs consequent to abrupt movement of a contrast boundary before the stationary eye. Thus, source 2. is effective, and its neurophysiological basis has been confirmed (Adey and Noda, i973; Jeannerod and Chouvet, 1973; Noda, 1975) in experiments on the lateral geniculate body of the cat. In view of this it may be asked whether source 3. might well be superfluous and, indeed, the evidence for its existence has been contradictory (see MacKay, 1973; Matin, 1974; and below). Our interest in this topic arose from the observation that each SEM is usually accompanied by a "spike" in the E E G of striate cortex in totally blind monkeys, and similar "spikes" are present even in the absence of eye muscles (Sakakura and Doty, 1976). It was also noted that transmission through the lateral geniculate nucleus (LGN) of alert, normal monkeys fluctuated rapidly, and that such fluctuation could be produced in sedated animals by electrical stimulation of pontine or mesencephalic reticular formation (Bartlett and Doty, 1974; Bartlett et al., 1973; Doty et al., 1973, Wilson et al., 1973). Putting these facts together, it was hypothesized that the visual world is examined in a cinematographic series of discrete samples as evidenced by successive ocular saccades and fixational pauses (see Gaarder, 1968); and that this sampling is aided by related central processes which act as a temporal framing mechanism

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by suppressing the relatively noninformative input generated by each SEM and f a c i l i t a t i n g t r a n s m i s s i o n at t h e o n s e t o f f i x a t i o n a l p a u s e s ( D o t y et al., 1 9 7 3 ) . T h e d a t a r e p o r t e d h e r e i n a r e at l e a s t c o n c o r d a n t w i t h s u c h a n h y p o t h e s i s . T h e y also s h o w t h a t , in a d d i t i o n to t h e l i k e l i h o o d o f a m a j o r c o n t r i b u t i o n f r o m M a c K a y ' s s o u r c e 2. a b o v e , t h e r e is a c e n t r a l l y o p e r a t i v e m o d u l a t i o n as p e r s o u r c e 3. I n o t h e r w o r d s , e x c i t a b i l i t y o f t h e c e n t r a l v i s u a l s y s t e m is s h o w n to f l u c t u a t e in r e l a t i o n to S E M s , e v e n w h e n t h e y o c c u r in a b s o l u t e d a r k n e s s ( D o t y et al., 1 9 7 4 ) .

Methods Nine macaques (M. nernestrina or M. fascicularis) and five squirrel monkeys (Saimiri sciureus) were used. Side-by-side electrodes with 0.5-mm tip exposure and 1- or 2-mm tip separation, were made from 0.2-ram diameter platinum-iridium or gold-plated nichrome wire. Under electrophysiological control and using aseptic surgical technique they were permanently placed in optic tract (OT), lateral geniculate nucleus (LGN), optic radiation (OR) and striate cortex. Horizontal and vertical electro-oculogram (EOG) components were eapacitatively recorded (typically 1.0 Hz-2 kHz bandpass) from 000-120 (1 • 3 ram) stainless steel screws implanted in periorbital bone. Electrode lead wires were brought to a miniature electrical connector affixed to the skull by medical grade methacrylate. All patently or potentially painful procedures, including insertion of ocular contact lenses, were always carried out under adequate anesthesia, and electrical stimulation was carefully evaluated for possibly noxious effects prior to experimentation. For recording sessions the animals were captured and restrained in a comfortable primate chair, in which they not infrequently dozed. Except as noted, amplifying and recording apparatus was conventional. Constant current was used for critical tests and for all conditions where continual stimulation was employed. The location of stimulating and recording electrodes in the central visual system was ultimately verified histologically. Data Collection and Analysis. To evaluate saccade related changes in central visual system excitability OT, LGN, or OR were electrically stimulated at various times closely preceding and following the onset of spontaneously occurring saccades, and at times remote from saccade onset. Stimulation was always submaximal and the amplitude of potentials evoked in OR or striate cortex served as the measure of excitability. The occurrence of saccades, taken in most cases as deflections of the horizontal EOG (temporal electrodes), was registered electronically by a voltage comparator circuit (Schmitt trigger) capable of detecting either positive, negative or both positive and negative EOG deflections. Through careful signal conditioning only the smallest saccades, roughly 1~ visually discernable in CRO displayed EOG recordings, escaped detection by this device. However, because of differences in the velocity of saecades, the range of error between the time when the onset of saccades could be visually detected in the EOG and the time when the comparator registered the occurrence of a saccade was about 15-20 msec. Data were collected using two different methods of electrical stimulation. In the first method electronic detection of a saccade activated an adjustable time-delay circuit which then triggered the electrical stimulation of OT or OR. Stimulation remote from the onset of saccades was triggered either manually or by a second circuit set for a post-saeeade delay of 400 or 500 msec. The 200-500 msec interval following saccade onset was explored in 5-20 msee steps, and evoked potentials were recorded either photographically or averaged by a computer of average transients (Cat 1000, Mnemetron Corp.). Photographic records were measured manually after enlargement. The second method employed continual stimulation of OT, LGN or OR at 50 or 20 Hz and recordings of the potentials evoked by this stimulation, the EOGs and stimulus markers, on a 7-channel Honeywell 7600 tape recorder. This method had several advantages over the preceding one. Both long and short term, nonsaccade related changes in excitability could be easily detected. In addition, by electronic manipulation of the recorded data, events occurring both before as well as after the onset of saccades could be evaluated. The main disadvantage of this "tetanization" was that time resolution was limited to either 20 or 50 msec (50 Hz and 20 Hz conditions respectively)

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becaus e of the asynchrony between the stimulus pulses and the occurrence of saccades. For example, in the 50 Hz case OT stimulation could follow any given saccade from 0 to 19.9 msec. Consequently, any statement about events occurring during periods following (or preceding) the detection of saccades has to be in terms of the average event occurring during the first, second, third, etc. 20-msec period that follows a given number of saccades. This tends to blur the onset and decreases the apparent magnitude of rapidly changing events (Fig. 2). Careful analysis showed no tendency for saccades to be time-locked to the stimulation of either OT, LGN or OR, nor for there to be a greater or lesser number of saccades during tetanization as compared with periods of no stimulation. Intermittent bouts of nystagmus were seen during continual OT or OR stimulation in darkness. However, nystagmus is also seen in darkness in the absence of central stimulation (H6rnsten et al., 1973; Skavenski and Robinson, 1973; Sakakura and Doty, 1976). There was no evidence that tetanization of OT elicited nystagmus in monkeys, although it does so in rabbits (Gutman et al., 1963). In any event, periods in which nystagmus occurred were excluded from analysis. From a technical standpoint, continual stimulation was a problem because stimulus artifact appeared in almost all EOG recordings and special electronic circuits had to be designed to ensure that these did not produce false triggering of the saccade detecting circuitry. Blinks were eliminated from data analysis when records were analysed by hand but not when computer averaging was used. In the latter case various estimates based on blink frequency versus saccade frequency showed that blinks produced only a minimal contamination of averaged data. Where data were tape recorded, analysis was limited to saccades that were not preceded within 250 msec by other saccades. Visual Conditions. Experiments were conducted under three visual conditions: 1. a well lighted (photopic range) patterned field, 2. a diffuse homogeneous field similar if not identical to a Ganzfeld and 3. complete darkness. All animals were tested under conditions 1 and 3 and four animals were tested under all three conditions. For some animals the "pattern" condition was a full view of the experimental chamber while for others it was a view of a 56~ ~ field of 0.17 cycles per degree black and white stripes whose contrast ratio was 1.58 log units. The white stripes had a luminance of 1500 cd/m 2. For the "diffuse" condition, the monkeys wore opalescent contact lenses and faced a white, shadowless, 56~ 64 ~ cardboard screen whose luminance was also 1500 cd/m 2. The contact lenses were manufactured by Wesley-Jessen Contact Lens Co., Chicago, Ill. to specifications obtained from keratometry on several macaques and squirrel monkeys. These normally clear lenses were made permanently opalescent by several coats of Type 126 Sapolin "Glass Frosting" spray paint (Sapolin Paints, Inc., New York, N.Y.) dried at 45~ for 24 hrs. The opalescent lenses produced about 0.8 log units of attenuation. The plain cardboard viewed through the opalescent lenses and the pattern of black and white stripes seen without the lenses thus have roughly the same average luminance; but, of course, the luminance of the white surface seen through the lenses is still 0.8 log units less than for the unobstructed view of the white stripes. Pupils were constricted with pilocarpine to eliminate the possibility of unobscured vision in the case of lens slippage. The guard hairs around the eyes were clipped to preclude their casting shadows. For comparison, pilocarpine was also used for the pattern and dark conditions in those four cases where animals were tested under all three conditions. While wearing the opalescent lenses, the animals showed no signs of detecting even moving stimuli unless the movement cast a transient shadow over its face. Dr. Y. Kayama, working in this laboratory, has placed these opalescent lenses on his own eyes and reports the sensation of a bright, textureless field except when looking directly into the unstopped beam of a 500 W slide projector, which makes slight imperfections visible. During all three visual conditions animals became drowsy but were not allowed to sleep. Sleep is easily detected by a decrease in saccade frequency (Biittner and Fuchs, 1973). In darkness this correlation was confirmed by observing animals with an infra-red "sniper scope". Various auditory or tactile stimuli were used to maintain as even a state of alertness as possible. Data collected during intentional "wake up" periods were not included in final data analysis.

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Results

Background Observations. Changes in amplitude of potentials evoked by stimulation of O T or O R were analyzed in relation to SEMs using three somewhat different methods. All three gave comparable results. The first analyses were m a d e by measuring individual potentials evoked by single pulses triggered at various selected times after onset of a SEM. The second method of analysis was similar except that the e v o k e d potentials were " a v e r a g e d " by computer (Table 1). In the third method the potentials were also " a v e r a g e d " by computer but were evoked continuously by 20 or 50 Hz stimulation (Figs. 1, 2, 6) and hence not precisely locked to the SEMs. Table 1. Comparison of saccade related suppression of magno- and parvocellular components of

potentials evoked in OR during pattern vision and during darkness. Averages for five macaques with range of averaged values in brackets. Percent suppression - maximum decrease in amplitude of OR potentials evoked by OT stimulation shortly after the onset of saccades, compared with the amplitude of similar potentials evoked at least 200 msec after onset of the same saccades. Latencies are for the time between the onset of saccades and the time of the indicated maximum suppression. Data for each animal were obtained by single pulse stimulation of OT at selected times following onset of saccades. The 200-msee interval following saceade onset was explored in 5-10 msec steps with data from 20-50 saccades being averaged for each step. "Pattern" signifies normally lighted experimental chamber; "Dark", complete darkness Magnocellular Maximum Suppression Latency (%) (msec)

Parvocellular Maximum Suppression Latency (%) (msec)

Pattern

43

30

17

Dark

(35-54) 14 (8-19)

(20-38) 68 (50-98)

(14-21) 8 (5-12)

44 (25-60) 48 (35-88)

As noted previously (Fentress and Doty, 1971), tetanization of O T or O R in primates can produce severe fatigue of synaptic processes. However, at 20 or even 50 Hz the fatigue is m o d e r a t e even for stimulation of O R (Fig. 1) for several minutes. These frequencies effected little change in the form of the response compared with that at 1 Hz; and it remained constant, though usually somewhat diminished, throughout the 5 - 2 0 min required for an experimental run. More troublesome was the " C h a n g effect" (Chang, 1952; Bartlett et al., 1973) which in some animals (electrode placements?) m a d e it difficult to analyze the later components of the response in striate cortex to stimulation of O R since these components almost disappeared in darkness. There was often a reverse effect for transmission through L G N , but it was minor, the basic response in O R for stimulation of O T being about 10% larger in dark than in patterned or diffuse light. It was important to establish the efficiency of the opalescent contact lenses and evenly illuminated white cardboard in producing a Ganzfeld, i.e., pattern-

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PATTERN

DAR K

A

B

OR

k_ C

D

17

Fig. 1. Excitability changes at OR and striate cortex during a single saccade. Macaque S-559. A, B Seven sequential potentials (right-hand traces, reading bottom to top) evoked in OR by continual 50-Hz, 0.07-msec, 1-mA stimulation of OT during single saccade shown as left-hand EOG recording (time vertical). A Animal viewing normally lighted experimental chamber; B Animal in darkness. Time of OT stimulation eliciting corresponding right-hand responses shown by dots (beam brightening) on EOG record. Calibration: EOG traces, 20 msec (vertical), horizontal uncalibrated. OR potentials, 50 ~tV/1 msec with onset delayed 0.9 msec to avoid registering stimulus artefact. C, D Same as A and B except seven right-hand traces are potentials evoked at striate cortex (area 17) by continual 50-Hz, 0.07-msec, 3-mA stimulation of OR. Calibration: EOG traces, as A and B. Striate potentials, 50 ~V/2 msec with 0.9 msec delayed onset. It is obvious that SEMs in darkness produce effects which in the single instance are equivocal, while in patterned light the changes are readily apparent. Potentials evoked at striate cortex have "atypical" waveform, suggesting poor alignment of stimulating and recording electrodes

less vision. This was d o n e b y s h o w i n g an a b s e n c e o f i n p u t o v e r O T in r e l a t i o n to s a c c a d e s in this c o n d i t i o n (e. g., Fig. 4), o r e v e n w h e n t h e o p a l e s c e n t lenses were worn and the illuminated, striped pattern presented rather than the blank c a r d b o a r d . T h e r e was also n o significant d i f f e r e n c e in t h e effects of S E M s on t h e e v o k e d p o t e n t i a l s (Figs. 2, 5) for t h e c o n d i t i o n s of b l a n k versus s t r i p e d c a r d b o a r d b a c k g r o u n d so long as t h e lenses w e r e in place, w h e r e a s t h e r e was a l a r g e difference in t h e i r absence. I n m a c a q u e s two c o m p o n e n t s c o u l d r e a d i l y b e d i s t i n g u i s h e d in t h e r e s p o n s e to s t i m u l a t i o n o f r o s t r a l O T as r e c o r d e d in O R (Figs. 1, 2). F o l l o w i n g p r e v i o u s a n a l y s e s ( D o t y et al., 1964; F e n t r e s s a n d D o t y , 1971; D o t y et al., 1973), t h e e a r l y a n d late c o m p o n e n t s a r e a t t r i b u t e d to a c t i v a t i o n o f t h e m a g n o c e l l u l a r a n d p a r v o c e l l u l a r e l e m e n t s , r e s p e c t i v e l y , o f t h e L G N . It was less c o m m o n to h a v e

Ocular Saccades and Visual System Excitability MAGNO

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Fig. 2. Percentage change in averaged (N = 100) peak-to-peak amplitude of "magnocellular" (G) and "parvocellular" (H) response components recorded in anterior OR of macaque S-825 before, during (arrows) and following SEMs that occurred f00 times in each of three conditions: Pattern, animal viewing central area of 56~ x 64~ black-white striped field; Diffuse, viewing central area of same size plain white field and wearing opalescent contact lenses; Dark, animal in complete darkness. Response evoked in OR by continual 20-Hz, 0.1-msec, 1.4-mA stimulation of anterior OT. Each histogram bin (A-F) represents average of 100 evoked potentials and a time period of 50 msee. Numbers (A-F) are percentage decrease from average inter-saccade values for each sample. Eye movement always present during period marked by arrow but start of movement varied between this and preceding bin. End of movements occurred in following two bins. In G and H lower trace deflection and brightening of upper trace include respective response peaks used for peak-to-peak measurements; true latency seen on lower trace, where upper obscured by stimulus artifact. Calibration: A-F, 10%/200 msec; G and H, 40 ~tV/0.5 msec

s t i m u l a t i n g a n d r e c o r d i n g e l e c t r o d e s a p p r o p r i a t e l y a l i g n e d to m a k e this distinction in squirrel m o n k e y s , b u t w h e n it c o u l d b e m a d e , t h e effects o f S E M s o n t h e s e c o m p o n e n t s w e r e the s a m e as in m a c a q u e s . I n d e e d , t h e r e a p p e a r to b e n o significant d i f f e r e n c e s in t h e m o d u l a t i o n o f excitability o f t h e c e n t r a l visual s y s t e m b y S E M s for t h e t h r e e species studied. Changes in Transmission Through L G N in Relation to SEMs. D u r i n g a n d a f t e r S E M s t h e p o t e n t i a l s e v o k e d in O R b y s t i m u l a t i o n o f O T w e r e , o n t h e a v e r a g e , s m a l l e r t h a n t h o s e e v o k e d b e t w e e n saccades. This " s u p p r e s s i o n " o f L G N t r a n s m i s s i o n o c c u r r e d in all a n i m a l s ; b e i n g m o s t m a r k e d d u r i n g p a t t e r n vision, c l e a r l y p r e s e n t b u t less m a r k e d d u r i n g diffuse, p a t t e r n l e s s ( r e d u c e d ) , i l l u m i n a t i o n a n d d e t e c t a b l e o n l y b y d a t a a v e r a g i n g w h e n a n i m a l s w e r e in a b s o l u t e d a r k n e s s (Figs. 1 - 3 ) . W h e r e b o t h m a g n o - a n d p a r v o c e l l u l a r c o m p o n e n t s o f t h e e v o k e d O R r e s p o n s e c o u l d b e satisfactorily r e s o l v e d , the m a g n o c e l l u l a r c o m p o n e n t was always t h e m o s t s u p p r e s s e d w h e n a n i m a l s v i e w e d e i t h e r t h e p a t -

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terned or diffuse fields (Table 1; Figs. 1, 2). In darkness this distinction was somewhat equivocal since both components were only minimally suppressed, and not until data for 20 or more saccades were averaged by computer or from photographic records could a small, but consistent, suppression be confirmed. Following the suppression, an enhancement of both magno- and parvocellular components occurred in several animals during all three visual conditions. While obviously a real phenomenon (e.g., Fig. 3), it was always small (5-15 %), and labile in that it was not consistently present to the same degree in the same animal under identical conditions. As can be inferred from Figs. 2 and 3, and Table 1, the time of onset and duration of the suppression varied greatly both between and within animals. In some cases it appeared to start prior to the SEM, most often in darkness or Ganzfeld (Fig. 2B, C, E, F). Since SEMs under the latter conditions (see also Adey and Noda, 1973; Riggs et al., 1974) tend to have lesser velocity than during pattern vision, it is possible that the seeming "presaccadic" suppression is an artifact arising from the later triggering of the SEM detector circuit by a slower rise time of the EOG. On the average, the suppression began close to or at the onset of the SEM, and then followed a variable time course which lasted up to 200 msec, except when interrupted by enhancement which also terminated by about 200 msec. The difference in magnitude and latency of the effect for magno- versus parvocellular components (Table 1)was statistically significant (Analysis of Variance: p < 0.01), as was the difference between visual conditions in each case. It must be emphasized that the data in Table 1 and Fig. 2 are averages and consequently cannot convey the variability of the suppressive effect. Identifiable suppression did not accompany every eye movement even during pattern vision (Fig. 3). Both decreases and increases in evoked potentials were seen in the absence of detectable eye movements, although for individual animals potentials falling in the lowest 25 % of the amplitude distribution were accompanied by a saccade 98% of the time. Further details of the variability as well as the transition from suppression to enhancement, for an animal in darkness, can be seen in Fig. 3. It is immediately clear here (Fig. 3) that the distributions D, E and probably F cannot be adequately represented by an "average", and that measures of "central tendency", e.g., standard deviation, are both meaningless and misleading. These bimodal distributions arise from the fact that, relative to SEM detection, the duration of LGN "suppression" (A-C) is not the same for all SEMs. For some, suppression gives way to enhancement between 60-79 msec after SEM detection (D) while for others this reversal does not occur until between 80 and 119 msec (E and F). As indicated by the absence of values around the median of the inter-saccade distribution (H), this reversal apparently contains no intermediate step, i.e., enhancement immediately follows suppression. Using the median of the intersaccadic distribution as a criterion, there is no evidence for suppression during at least 10% of the 264 SEMs (Fig. 3A-C), and probably the same number fail to show enhancement (Fig. 3G). These numbers are, of course, increased if the standard deviation of the distribution is used as criterion. However, statistically (p < 0.01, Chi 2 test) each of the dis-

Ocular Saccades and Visual System Excitability

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Fig. 3. Details of excitability changes related to SEMs in the dark. A - G Peak-to-peak amplitude distributions for 264 magnocellular potentials evoked in OR during designated successive 20-msec periods following onset (A) of 264 saccades generated in complete darkness by macaque M-605. H Amplitude distribution of 12 055 similar potentials evoked between the same 264 saecades but at least 250 msec from their onset. OR potentials evoked by continual 50-I-Iz, 0.07-msec, 3-mA stimulation of OT. Dashed lines indicate bin containing median (and mean) of intersaccade distribution H. Percentage of 264 amplitudes falling to each side of this value are given for each distribution A-G. Average saeeade rate, 1.13/see; total sample time about 4 min 53 see. It is apparent that there is a biphasic shift in the distribution of amplitudes in relation to the saccades. The abruptness of the shift (C, D, E) is probably attenuated by the play in triggering time for each saccade (see Method). The few extreme values for distribution in H may well result from SEMs too small to have been detected

tributions A - G are different from the intersaccade distribution ( H ) and this establishes b e y o n d r e a s o n a b l e d o u b t that L G N transmission during S E M s is n o t the s a m e as that occurring b e t w e e n S E M s e v e n w h e n visual input is absent. D a t a analysis o f this type was u s e d for all o f the less certain effects r e v e a l e d by data averaging.

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Neither magnitude nor direction of the SEM seemed to influence the magnitude of suppression or enhancement. The analysis performed on this question, howev.er, was not sufficiently extensive to be considered definitive. Changes in Excitability of Striate Cortex in Relation to SEMs. In three macaques and one squirrel monkey an effort was made to study the effects of SEMs on potentials evoked at striate cortex by stimulation of OR. This was made difficult by considerable between-animal differences in the waveforms of the evoked potentials and by moment to moment changes in waveform (e.g., Fig. 6) within the same animal. Because of these problems it cannot be said with certainty that the same events were measured in each animal. For these experiments the paradigm was identical to that used to test LGN transmission. Tetanization at 20 or 50 Hz was used in all cases and all data were analyzed primarily by computer averaging. For about 40-60 msec following detection of SEMs the average amplitude of early, but postsynaptic, potentials (Doty et al., 1964) evoked at striate cortex was less than that for potentials evoked before or at times remote from SEM occurrence. This suppression was small (4-17 %) but occurred in all animals during both pattern vision and darkness. The latency between SEM detection and peak suppression was between 30-100 msec for pattern vision and 40-60 msec in darkness. Beginning about 60-100 msec after SEM detection the average amplitude of potentials increased, sometimes dramatically (Fig. 1C). The largest increases occurred during pattern vision; the average enhancement being about 64% (range 11-122%) in pattern vision and about 15% (range 0-21%) in darkness., The one squirrel monkey (21-1X-73) was the only animal which failed to show convincing enhancement in darkness and it was also the animal with the least~enhancement during pattern vision - probably because of the peculiarity of its evoked potentials (see Sakakura and Dory, 1976). Like the preceding suppression, the latency to the peak of enhancement was greater (150-200 msec) in darkness than in pattern vision (100-150 msec). Besides being tested during pattern vision and darkness the one squirrel monkey and macaque S-825 were also tested during diffuse illumination. For both animals this condition was equivalent to pattern vision. In fact, for the squirrel monkey, enhancement was somewhat greater (17 vs 11%) in diffuse illumination than during pattern vision. The caveats concerning data averaging that were pointed out earlier are also applicable to the present data which, as just mentioned, also suffer from other problems. None the less, there is little doubt that excitability at striate cortex is, in most cases, altered during SEMs regardless of whether or not the eye movement results in a change of retinal excitation. Potentials in 07, L G N and Striate Cortex Occurring Inherently in Relation to SEMs. As described by Feldman and Cohen (1968; also Cohen and Feldman, 1971) and repeatedly confirmed in this laboratory (e.g., Sakakura and Doty, 1976), SEMs in monkeys are commonly followed by a clear, abrupt potential in LGN and striate cortex, even when the SEM occurs in the dark or in the blind animal. This phenomenon was also studied briefly in the present experiments (Figs. 4, 5) in one macaque (S-825) and one squirrel monkey (21-1X-73).

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In both animals the potentials in striate cortex were readily observable for single occurrences, but in OT and OR data averaging was required. This demonstrated that no response occurred in OT in relation to SEMs in darkness or Ganzfeld (Fig. 4), whereas there was a potential in OR (probably to some degree recorded electrotonically from LGN) and striate cortex under these conditions (Fig. 4). The average latencies of the potentials at LGN, OR and striate cortex relative to onset of the SEM were clearly related to presence or absence of illumination. For pattern, diffuse and dark conditions the average latency at OR was 10, 15 and 35 msec for the squirrel monkey and, at LGN, 15, 15 and 37 msec for macaque. Comparable values at striate cortex were 40, 60 and 130 msec for squirrel monkey and 39, 63 and 118 msec for macaque. In pattern vision and in contrast to the "10 msec" latency at OR, the average latency of squirrel monkey OT potentials was about 30 msec, i.e., potentials were detected about 20 msec earlier in OR than in OT. Obviously, the 10 msec latency in OR may reflect an artifactual shortening because of delayed triggering on the SEM; but since the trigger level was the same for the same SEMs in averaging the OT and OR data, the relative difference must be accepted. The "average" amplitude was only slightly reduced in diffuse as compared to patterned light, but greatly diminished in darkness (e. g., Fig. 4). However, as shown in Fig. 5, these reductions are more apparent than real, since they result from variations in latency which distort the "averaging" process. Even Fig. 5, however, fails to give the entire picture. Some of the variability in latency in the dark appeared to be attributable to the relatively large number of instances in which one saccade was followed immediately by another, smaller saccade (see Becker and Fuchs, 1969). In these cases the latency relative to the

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first saccade was longer than when only one saccade was made. This suggests that the potential in striate cortex is correlated more with the end of an SEM than its onset, a possibility also considered by Feldman and Cohen (1968) in the macaque LGN, and by Munson and Schwartz (1972) and Sakai (1973) for LGN and visual cortex in the cat. The double saccade, however, accounts for only a part of the decrease in average amplitude in darkness (Fig. 4). In analyzing the data for Fig. 5 it was found that detectable potentials followed only 58% of the SEMs made in darkness, where the corresponding figures for diffuse and patterned light were 78% and 85%, respectively. It thus cannot be stated to what degree variation in amplitude, latency or even presence or absence of response contributed to the "averages" obtained in Fig. 4. Changes in Geniculo-Striate Excitability Independent of SEMs. Alterations in attentive state, occurring naturally or through stimulation of pontine or mesencephalic reticular formation, produce large changes in excitability of the central visual system in monkeys (Doty et al., 1964; Bartlett et al., 1973; Wil-

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son et al., 1973; Bartlett and Doty, 1974; Sakakura and Doty, 1976). These effects are as large and often larger than any seen in relation to SEMs. A typical comparison can be seen in Fig. 1 versus Fig. 6, taken from the same m a caque. In Fig. 6 no SEMs had b e e n detectable in either vertical or horizontal E O G for about 30 sec. This absence continued throughout the 1 sec sample shown, but SEMs were resumed almost immediately thereafter. It is thus highly probable that Fig. 6 represents a spontaneous transition from a drowsy to an alert state, since no deliberate stimulus was givenl and the m o n k e y in this instance was isolated in a soundproof chamber. As may be judged from the great change in waveform within 20 msec (e.g., Fig. 6, C-8, D-8, E-8, A-9), this transition is accompanied by very rapid and complex fluctuations in the state of the geniculostriate system. To avoid such effects the animals were deliberately kept alert while the influence of SEMs was being recorded. However, smaller, undecipherable changes still occurred, as can be seen in Fig. 7. In Fig. 7B an absence of SEMs is associated with a reduction in variability of the response when the m o n k e y is in a patterned environment. However, in the dark such stability can occur in the presence of eye m o v e m e n t s (first third of Fig. 7A), and large transitions (Fig. 7A) or slow, quasi-rhythmic fluctuations at about 0.05-0.03 Hz can occur without discernible relation to SEMs (Fig. 7A, C).

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Fig. 7. Subtle changes in excitability only partly related to SEMs. Spontaneous, sometimes slowly rhythmic variations in the amplitude of potentials evoked in OR of macaque S-825 (A and B) and squirrel monkey 21-1X-73 (C) by continual 20-Hz stimulation of OT. Number of concurrent SEMs also summarized for A and B. Although not illustrated, SEMs showed no correlation with fluctuations in C. A, C Animals in complete darkness9 B Animal viewed central area of 56~ ~ black-white striped field. OT stimulation: A, B, 0.1 msec, 1.4 mA; C, 0.1 msec, I mA. Each point represents either the average peak-to-peak amplitude of ten consecutively evoked potentials (time period equal to 0.5 sec) or the number of SEMs occurring in 0.5 sec. Total of each record, 4 min 16 see. Maximum number of saccades occurring in 0.5-sec period, four. Circled dot in A belongs to top record. Note for B the essential absence of variation during periods with no eye movements

F r o m Fig. 7 it m a y b e i n f e r r e d t h a t t h e G a u s s i a n d i s t r i b u t i o n o f a m p l i t u d e s s e e n in Fig. 3 H p r o b a b l y d o e s n o t r e p r e s e n t a r a n d o m d i s t r i b u t i o n a r o u n d a fixed m e a n b u t i n s t e a d reflects v a r i a t i o n a r o u n d a set o f m e a n values. This s u p p o s i t i o n is s u p p o r t e d b y t h e fact t h a t t h e d i s t r i b u t i o n o f i n t e r s a c c a d e a m p l i t u d e s a p p r o a c h e s G a u s s i a n f o r m o n l y w h e n r e l a t i v e l y large s a m p l e s a r e analyzed. Frequency of SEMs. R a t e o f o c c u r r e n c e o f S E M s was s t u d i e d in f o u r m a c a q u e s a n d o n e squirrel m o n k e y to specify h o w it c h a n g e d u n d e r t h e t h r e e visual c o n ditions e m p l o y e d 9 I n all cases t h e r a t e was l o w e s t in the d a r k a n d h i g h e s t with p a t t e r n vision. U s i n g 5 - m i n s a m p l e s a n d e x c l u d i n g a n y r e c o r d s in which nyst a g m u s o c c u r r e d , t h e a v e r a g e for t h e m a c a q u e s was 1.77 S E M s / s e c in p a t t e r n e d light ( r a n g e 3 . 1 5 - 1 9 a n d 0.79 S E M s / s e c in t h e d a r k ( r a n g e 1 . 1 3 - 0 . 2 6 ) . F o r t h e s q u i r r e l m o n k e y o n d i f f e r e n t d a y s t h e a v e r a g e in p a t t e r n e d

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light was 1.58 SEMs/sec (range 1.76-1.41), and 1.10 SEMs/sec in the dark (range 1.21-0.98). For none of these five animals nor for others tested was there a statistically significant difference between frequency of SEMs with and without tetanization of OT or OR. Incidental observations confirmed the fact that velocity of saccades tends to be slower in darkness (Adey and Noda, 1973; Becker and Fuchs, 1969; Riggs et al., 1974), and that blinks are always accompanied by an upward saccade (Bell's phenomenon). The frequency of SEMs seemed directly related to the "emotional state" of the monkey, being high along with other motor activity. The opalescent contact lenses had a remarkable tranquilizing effect and in all cases reduced the frequency of SEMs relative to that with normal vision. In some cases, particularly in the squirrel monkey, the rate of SEMs was about the same in this Ganzfeld condition as in darkness. The "average" rate, obviously, does not specify fully the changes in occurrence of SEMs in the three conditions of vision. Figure 8 presents an analysis of intersaccadic intervals, comparing the macaque and squirrel monkey. Nota-

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ble here is the marked increase in variation of intersaccadic intervals in darkness versus light; and the fact that the macaque has a greater change than the squirrel monkey, and shows a greater difference between Ganzfeld and pattern vision. While these data suggest the possibility that animals or species might have unique features in the distribution of their intersaccadic intervals under various conditions of vision, it is more likely that these distributions would undergo considerable change as motivation, novelty, etc. fluctuate from day to day. In what way, if any, such differences in saccadic behavior are related to the other phenomena reported here is unknown. Discussion

Centrally Originating Modulation. These experiments establish unequivocally that there is a modulation of neuronal excitability in the central visual system consequent to SEMs executed in total darkness. Since there is no evidence (e. g., Fig. 4) for retinal discharge in relation to saccades in darkness, nor any evidence that proprioceptive feedback from extraocular muscles has any influence on the geniculostriate system (e.g., Orban et al., 1972), it seems reasonable to assume a central origin for this modulation. The psychophysical counterpart of these experiments, performed by Riggs et al. (1974), using electrically elicited phosphenes in man, provides equally strong evidence that SEMs alter the excitability of the visual system through central processes. Thus, while entirely valid, the effects demonstrated by MacKay (1973), Mitrani et al. (1975), Adey and Noda (1973) and Jeannerod and Chouvet (1973), in which "saccadic suppression" can be attributed to the input generated by transit of patterns across the retina, cannot be considered the sole source for the modulation accompanying SEMs. Specifically, we assume that the centrally originating effects emanate from the pontine system (Cohen and Komatsuzaki, 1972; but see Lynch et al., 1975; Yin et al., 1975) which generates the SEM; parallel outputs passing from it to the oculomotor and visual systems. This assumption is buttressed by a number of facts. Effects on transmission through the LGN, similar to those found in association with SEMs, can be obtained by electrical stimulation of the pontine and mesencephalic reticular formation (Wilson et al., 1973); and Cohen and Feldman (1968) showed that the stimulation of the pontine focus eliciting SEMs also evoked potentials in the macaque LGN similar to those which occur with each natural SEM. In the cat the ponto-geniculate-occipital (PGO) spikes, seen not only in the rapid eye movement phase of sleep but also with ocular saccades in the alert animal (Bizzi, 1966; Brooks and Gershon, 1971; Corazza and Lombroso, 1971; Jeannerod, 1972; Munson and Schwartz, 1972; Sakai, 1973), are triggered by pontine stimulation (Bizzi and Brooks, 1963; Brooks and Gershon, 1971; Munson et al., 1975; Orban et al., 1972; Singer and Bedworth, 1974; and see Laurent, Guerrero and Jouvet, 1974). While sometimes differing in detail, the PGO spikes of sleep and those observed in the alert animal seem likely to have a common pontine origin. A common origin can also be inferred for the potentials (Figs. 4, 5) and for the changes in excitability (Figs. 1-3) seen in LGN and striate cortex following

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SEMs. Both have similar latencies and are similarly affected by changes in visual state (patterned light, Ganzfeld, darkness). The fundamental nature of these effects is seen not only by their prevalence and persistence in blindness (Bizzi, 1966; Sakakura and Doty, 1976), but by the fact that they develop both in cats (Vital-Durand and Jeannerod, 1975) and macaques (Doty and Negrfio, to be published) that have been deprived of visual experience since birth. Discrepancies. The failure of Biittner and Fuchs (1973) to find any alteration related to SEMs in 95 % of the LGN units they studied, an observation now confirmed by Duffy and Burchfiel (1975), seems wholly discordant with the results reported here. It must be recalled, however, that in darkness, the condition of the Biittner and Fuchs experiment, the effect of SEMs on LGN excitability may be only of the order of 5 - 1 0 % and thus possibly in agreement with the figure of 5 % for the number of LGN units they did find to be affected. Furthermore, the effect is greatest in the magnocellular elements, which constitute only 12% of the neurons in the primate LGN (Le Gros Clark, 1940; Doty et al., 1964). Their relatively small number plus their position ventral to the parvocellular mass, from which successful recording is readily obtained, probably biased the sample strongly against magnocellular elements in the Bfittner and Fuchs study. Since Biittner and Fuchs (1973) found a powerful coupling between SEMs and discharge in the pregeniculate nucleus, it must be asked whether this discharge could have contributed significantly to the records obtained in the present study. This cannot be answered with certainty, but a number of facts suggest it is unlikely. First the pregeniculate nucleus, so far as is known, does not project to the cortex. The changes in potentials recorded in OR, which we attribute to transmission through LGN, could be recorded many millimeters distant from the LGN and are thus unlikely to include serious contamination from events spread electrotonically from the pregeniculate nucleus. In addition, the potentials recorded in traverses through LGN by Feldman and Cohen (1968), occurring inherently in association with SEMs, bore no spatial distribution suggestive of a focus in the pregeniculate nucleus. More puzzling is the failure of Adey and Noda (1973; Noda, 1975) to find, in the dark, any influence of SEMs upon the LGN of the cat, despite the consistent reports of potentials appearing in LGN in association with SEMs (Bizzi, 1966; Bizzi and Brooks, 1963; Brooks and Gershon, 1971; Corazza and Lombroso, 1971; Jeannerod, 1972; Munson et al., 1975; Orban et al., 1972; Sakai, 1973; Singer and Bedworth, 1974). Failure by others can be attributed to inadequate methods, but Adey and Noda's procedures should have revealed the effects were they present, although the raw data were apparently not submitted to computer averaging, which proved so useful in the present experiments. On the other hand, Adey and Noda (1973) do not follow through the implications of their finding pronounced effects at the cortical level in the absence of any influence on the LGN. Such results demand an extrageniculate pathway, for which there is some evidence in the observations of Hobson et al. (1969) and Laurent, Cespuglio and Jouvet (1974). Furthermore, when excitability of the LGN was depressed by SEMs in the presence of visual patterns,

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the cortical response was also diminished (Adey and Noda, 1973). The relation between LGN and cortex is here opposite to that displayed in alterations of alertness, where a reciprocal relation prevails (Bartlett et al., 1973; Dagnino et al., 1965; Walsh and Cordeau, 1965). Comparable observations were made in the present experiments where concurrent changes in excitability of LGN and striate cortex appeared to be roughly similar, rather than reciprocal, following SEMs. By the use of signal averaging we have been able to record potentials in striate cortex associated with SEMs made in the dark, whereas Cohen and Feldman (1971) did not detect them in single samples. There are, howeve r, occasional placements in striate cortex from which these potentials can be recorded in darkness with consistency equal to the recording of Lambda waves associated with SEMs in patterned light (Sakakura and Doty, 1976). The same appears to be true for appropriate placements on the scalp in recording the comparable events from certain human subjects (Becker et al., 1972). The necessity for using computer averaging to reveal effects otherwise obscured by background activity - or, if inhibitory, requiring either high background or a long period of sampling, probably accounts for the inability of Wurtz (1969) to demonstrate any centrally originating influence of SEMs on units in striate cortex of alert macaques. However, it is also possible that the effect is dependent upon the behavioral conditions under which the SEMs are made (see Lynch et al., 1975). In Wurtz's experiments all SEMs were made for the same purpose by highly trained monkeys. This uniformity conceivably might have excluded the type of SEM in which the modulation of striate units is greatest. In any event, in addition to the report of Valleala (1968), Dully and Burchfiel (1975) and Kayama et al. (1975) have now found units in striate cortex in which the background rate of discharge is, on the average, increased or decreased in association with ad libitum SEMs made by macaques in complete darkness; and Robinson and Wurtz (1976) have discovered units in the superior colliculus which clearly differentiate between inputs generated by external movement versus SEMs. The difference in magnitude and timing of influence on magno- and parvocellular elements in LGN (Table 1) suggests that operations on these two systems are differentiated, although the significance of such differentiation is presently as unclear as is the functional significance of the magno- parvocellular division itself. As the data show, both components are modulated during SEMs and this is concordant with earlier data (Bartlett and Doty, 1974) showing that all types of units encountered in striate cortex could be influenced by appropriately localized electrical stimulation of the mesencephalon. Significance. Unfortunately, it cannot be discerned here whether the effects of SEMs on evoked potentials represent a small change in many elements or a large change in a few. From the work with single units in striate cortex (Dully and Burchfiel, 1975; Kayama et al., 1975) the former seems more likely, i.e., many units show a small change. However, the constraint of working with untrained monkeys held in darkness probably leads to a significant underestimation of what the true magnitude of the effect would be in a normal visual environment. In most instances, and especially for the magnocellular component

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(Figs. 1, 2), the effect is significantly stronger in diffuse light than in the dark. Were it possible 1. to have absolute confidence in the adequacy of the Ganzfeld (no blinking, no looking at limits of field, etc.), 2. to detect even the smallest SEMs, and 3. to compensate for variance in SEM triggering latency (Fig. 3), a much more substantial modulation than found in the present experiments might be revealed; more in line with the 30-fold increase in threshold estimated by Riggs et al. (1974) to originate centrally in relation to each SEM. A primary question is whether the effects reported here are specific to SEMs or whether instead they merely reflect a slight, momentary, general increase in alertness which might accompany many but not all SEMs. Schwartzbaum (1975) has found for the rat that activity in the LGN is altered by any type of movement; and Meulders and Godfraind (1969) have shown not only that somatosensory stimuli alter the response of units in the LGN of the cat but that the mesencephalic reticular system is essential for the effect. The only clue presently available for monkeys is that the reciprocal relation (Bartlett et al., 1973) between LGN and striate cortex in the changes they undergo in their excitability for transitions from the inattentive to the alert state and vice versa appears to be lacking for the modulation accompanying SEMs. In this vein, the latter thus would not seem to reflect an alerting effect, and the same holds for the cat (Adey and Noda, 1973; Dagnino et al., 1965; Walsh and Cordeau, 1965). On the other hand, SEMs are often m a d e t o stimuli which have a definite alerting effect, and in such case any modulation specifically related to SEMs per se would necessarily be intermixed with that from alerting. It is not known to what degree the present data are complicated by this factor and, indeed, it would be difficult, perhaps impossible, to design experiments which would effect a convincing separation of these factors. The central issue in these experiments is their relevance to the phenomenon of "saccadic suppression" and whether the latter in turn is related to the hypothesized "corollary discharge" for achieving a stable visual world from a fluctuating retinal image. There is now a plethora o f means for achieving saccadic suppression: 1. blinking, which commonly accompanies SEMs, particularly those of large amplitude (e.g., Hall, 1945; Haberich and Fischer, 1958): 2. retinal input consequent to the SEM (Adey and Noda, 1973; Jeannerod and Chouvet, 1973; MacKay, 1973; Mitrani et al., 1975; Noda, 1975); 3. the centrally originating modulation shown herein, for the cortex in the experiments of Adey and Noda (1973), and psychophysically in the experiments of Riggs et al. (1974). From the great increase in modulation seen with pattern vision compared with Ganzfeld (Fig. 2) it seems likely that the latter two effects summate (although the complication of reduction of the maximum level of illumination by the contact lenses used with our Ganzfeld should not be overlooked). Why there should be two or three means of achieving suppression, whether they actually summate, and whether they all subserve the same function, cannot presently be discerned. MacKay (1973) has cogently argued that suppression is not a necessary concomitant of the process which preserves visual stability in the face of constantly recurring SEMs. Whatever may be the actual case, two facts show

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unequivocally that events central to the retina are sufficient to initiate processes which achieve this stability, i.e., the suppressive effect from at least the retina is not required. When the eye is immobilized and a saccade attempted, the world appears to move (e.g., Brindley and Merton, 1960; Kornmiiller, 1931); and in the blind subject the absolutely fixated phosphene elicited by electrical stimulation of striate cortex appears to move in space concordantly with movement of the eyes (Brindley, 1973). The latter observation shows: a) that the modulation generated by an SEM is precisely encoded for direction of eye movement, and b) that it is probably effective upstream to striate cortex, although a possible involvement of corticogeniculate fibers (Hollander, 1974) is not excluded. While "corollary discharge" or "Efferenzkopie" are useful as brief phrases to allude to a complex phenomenon, it is apparent from the foregoing that they are meaningless so far as substantive explanation is concerned. The effects reported herein may or may not be related to the "corollary discharge", for the operations remain unknown and unspecified through which such discharge would achieve the visual stability it is intended to explain. Our present speculation concerning the effects we have observed runs along the following lines. Suppression is useful in averting the normally operative reflex of "acquiring" a moved or moving target; a "nonexistent" target in the case of input generated by an SEM (see Lynch et al., 1975). It would also attenuate and perhaps shorten the otherwise powerful input consequent to the SEM and thus permit earlier analysis of input received at the onset of a new fixation. The latter would, in addition, be hastened by the facilitation which is commonly observed to follow the suppression (e.g., Fig. 3). Such a sequence, well supported by the data herein, is clearly useful in the process of sequential visual sampling. However, the problem remains that suppression is by no means total, the enhancement is only moderate, and probably not all SEMs are accompanied by these effects (Fig. 3). Thus it seems likely that such a sequence of suppression and enhancement would often fail to distinguish external from self-generated movement; particularly if similar events (e.g., suppression) were generated by external movements alone. Such failures seldom occur and therefore the effects here, even though originating centrally and related to SEMs, seem inadequate by themselves to provide the clue for distinguishing the origin of gross movement of the visual field. References Adey, W.R., Noda, H.: Influence of eye movements on geniculo-striate excitability in the cat. J. Physiol. (Lond.) 235, 805-821 (1973) Bartlett, J.R., Doty, R.W., Sr.: Influence of mesencephalic stimulation on unit activity in striate cortex of squirrel monkeys. J. Neurophysiol. 37, 642-652 (1974) Bartlett, J.R., Doty, R.W., Pecci-Saavedra, J., Wilson, P.D.: Mesencephalic control of lateral geniculate nucleus in primates. III. Modifications with state of alertness. Exp. Brain Res. 18, 214-224 (1973) Becker, W., Fuchs, A.F.: Further properties of the human saceade system: eye movements and correction saccades with and without visual fixation points. Vision Res. 9, 1247-1258 (1969)

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Received November 25, 1975