TECTAL CODIFICATION OF EYE MOVEMENTS INGOLDFISH STUDIED BY ELECTRICAL

MICROSTIMULATION

C. SALAS,* L. HERRERO,† F. RODRIGUEZ* and B. TORRES†‡*Dpt. Psicologıa Experimental, Fac. Psicologıa, Univ. Sevilla, Avda. San Francisco Javier s/n,

41005 Sevilla, Spain

†Lab. Neurobiologıa, Dpto. Fisiologıa y Biologıa Animal, Fac. Biologıa, Univ. Sevilla, Avda. ReinaMercedes 6, 41012, Sevilla, Spain

Abstract––This work compares the tectal codification of eye movements in goldfish with those reported forother vertebrate groups. Focal electrical stimulation was applied in various tectal zones and thecharacteristics of evoked eye movements were examined as a function of (i) the position of the stimulationover the tectal surface, (ii) the initial position of the eyes and (iii) the parameters (pulse rate, currentstrength, duration) of the stimulus. In a large medial zone, stimulation within the intermediate and deeplayers of the tectum evoked contraversive saccades of both eyes, whose direction and amplitude wereroughly congruent with the retinotopic representation of the visual world within overlying layers. Thesesaccades were minimally influenced by the initial position of the eye in the orbit. The topographicalarrangement of evoked saccades and body movements suggests that this tectal zone triggers orientingresponses in a similar way to those described in other vertebrates. Stimulations applied within the caudaltectum also evoked contraversive saccades, but—in disagreement with the overlying retinotopic map—thevertical component was absent. Taken together with electrically evoked body movements reported infree-swimming fish, these saccades could reveal that this zone is involved in escape responses. Whenstimulations were applied within the anteromedial zone of the tectum, contraversive movements of botheyes appeared much more dependent on initial eye position. Saccades elicited from this area displayedcharacteristics of ‘‘goal-directed saccades’’ which were similar to those described in the cat. The generationof goal-directed movements from the anteromedial zone suggests that this portion of the goldfish optictectum has a different intrinsic organization or is connected with the brainstem saccade generator in adifferent fashion than the medial zone. Finally, stimulation of the extreme anteromedial zone evokedconvergent eye movements. These movements and those reported in free-swimming fish followingelectrical stimulation of this tectal area suggest that this zone could be involved in feeding responses.The relationships between the parameters of electrical stimulation and the characteristics of elicited

saccades suggest that the stimulated location within the tectum determines a constant direction in theevoked saccade, whereas the amount and duration of tectal activity, as mimicked by changes in stimulusparameters, together with the tectal locus, determine the velocity and amplitude of the evoked saccade.? 1997 IBRO. Published by Elsevier Science Ltd.

Key words: orienting response, saccadic generator, motor map, oculomotor system, superior colliculus,fish.

Robinson47 reported that microstimulation of thedeep collicular layers of head-fixed primates evokescontraversive conjugate eye saccades whose ampli-tude and direction depend on the stimulation site,revealing a motor map of eye movements that is incorrespondence with the overlying sensory map ofthe superficial layers. The alignment of the sensoryand motor maps was confirmed by combining re-cording and microstimulation techniques.52 Cellsin these collicular layers discharge vigorouslybefore the onset of saccadic eye movements, havingmetrical properties corresponding with their move-ment fields.28,52,57,67 Electrical microstimulation ofthese regions evokes short-latency saccadic eyemovements;17,47,52,65 lesions or pharmacological

manipulations lead to changes in saccadecharacteristics.16,22,26

Similar studies carried out in head-fixed cats dem-onstrated different patterns of saccadic movementsdepending on the rostrocaudal extent of the stimula-tion site.17,33,48 These differences were explained onthe basis of the restricted cat’s oculomotor range.45,48

Stimulating the superior colliculus in rodents sug-gests that this structure mediates either orientingresponses or defensive movements such as avoidanceor flight.5,6,32,43 Dean et al.6 suggested that in ani-mals such as rodents, with laterally placed eyes andwith a poorly developed central area in the retina, thesuperior colliculus can make intelligent decisions,which depend on stimulus characteristics, to generateorienting movements towards a novel stimulus or tomove away from it. In summary, it has been‡To whom correspondence should be addressed.

Pergamon

Neuroscience Vol. 78, No. 1, pp. 271–288, 1997Copyright ? 1997 IBRO. Published by Elsevier Science Ltd

Printed in Great Britain. All rights reserved0306–4522/97 $17.00+0.00PII: S0306-4522(96)00587-8

271

proposed that the role of the superior colliculusvaries markedly between species.6 A similar conclu-sion may also be reached from studies in the optictectum of birds,8 reptiles60 and amphibians.13

Although the way in which the fish optic tectumgenerates motor behaviors has occasionally beendescribed,1,2,36 its contribution to orienting eyemovements is virtually unknown. Physiologicalstudies on fish optic tectum are needed to betterunderstand how the functional properties of thisstructure have been modified over the course ofevolution to subserve adaptive changes in behavioralphenotypes. The goldfish seems to be a useful animalon which to perform this kind of comparative studybecause it exhibits an extensive repertoire of eyemovements,9,11,15 and the basic oculomotor circuitryis conserved from teleosts through to mam-mals.46,62,63 However, some of the features of thegoldfish’s visual system, which play a notable role inthe generation of orienting responses, contrastgreatly with those of primates and carnivores, andare similar to those of rodents. Goldfish are lateraleyed, and their large visual field spans up 280), butthe binocular overlap in goldfish is about 30).64

Furthermore, the goldfish lacks a true fovea, al-though the density of receptors is higher in its centralretina than in the periphery,21 which could be used toattend to objects of interest.10,68 These particularcharacteristics enhance the importance of the com-parative approach to determine whether the tectalcodification of eye movements in goldfish might differfrom or be similar to those in other vertebrates.Current hypotheses suggest that eye movement

characteristics are encoded in the superior colliculusand are dependent on both the location and par-ameters of electrical stimulation.45,54,59,65 In thisreport the following aspects have been studied: (i) thetectal map of evoked eye movements; (ii) the influ-ence of initial eye position on evoked saccades; (iii)the dependence of electrically evoked saccade metricson stimulus parameters. A brief preliminary report ofthese results has been published elsewhere.50

EXPERIMENTAL PROCEDURES

Animals and surgical preparation

Experiments were carried out on 11 goldfish (Carassiusauratus) of 15–20 cm body length obtained from localsuppliers. The animals were maintained in aquaria at 20)Cfor at least two weeks before any experiments.All experimental procedures were in accordance with the

guidelines for animal research established by the universityregulations on laboratory animal care. Under general an-esthesia (1:20,000 w/v, solution of tricaine methane-sulfonate), each animal was clamped firmly between twoplastic pads inside a home-made perspex water chamber.The mouth was fitted to a plastic tube connected to awell-aerated water circuit propelled by a pump to ensure aconstant flow over the gills. Anesthetic concentration in thewater circuit was maintained at a suitable level duringsurgical preparation of the animals, which included openinga hole through the skull and implanting coils on the eyes.The surgery was begun by cutting away a small area of the

cranium, dorsal to the midbrain, and gently removing theunderlying fat to avoid bleeding, until the tectal lobes wereclearly visible. To ensure head stability during recording,two thin rigid bars clamped the temporal bones of the fish tothe walls of the tank.Eye movements were recorded using the scleral search

coil technique. A 60-turn coil made of enamel-insulated25-µm copper wire (2.3 mm o.d.; Sokymat, Granges,Switzerland) was sutured to the upper scleral margin of eacheye. The tank containing the prepared fish was placedwithin the magnetic field with the animal’s eyes in thecenter. The diameter of the magnetic field coil was 30 cm.Eye movement calibrations were obtained by rotating themagnetic field coils at known angles (&5), 10), 15) and 20))around the stationary eye coil. Once the surgical procedurewas finished the water of the tank was changed, usuallythree to four times every 10 min, thus removing the anes-thetic. The animals recovered an alert state about 10–15 minfollowing the first change of water, as shown by there-establishment of the normal pattern of eye movements.51

When the experiments began, about 1 h after surgery, thezero eye position in the orbit was defined as the middle ofthe eye movement range after 15 min of spontaneous eyemovements. Repetition of this procedure at the end of theexperiment showed that the zero eye position did not driftthroughout the session. The electrical stimulus and recordsof eye movements were stored on videotape (Neuro-Corder,Neuro Data Instruments).

Electrical microstimulation

In preliminary experiments, electrical stimulation wascarried out with monopolar electrodes comprising stainlesssteel entomological needle minutiae insulated with twocoats of Epoxylite varnish. Insulation was removed fromthe needle tip to expose a tip estimated as 20–40 µm longand 10–20 µm wide. Because the insulation varnish of someof these microelectrodes sometimes appeared to deterioratefollowing their use, it was difficult to ascertain if theelectrical stimulation was localized in the intermediate anddeep tectal layers using these electrodes. Therefore, anothertype of glass-insulated stainless steel wire (25 µm diameter)microelectrode was used. So, although results were similarwith both types of microelectrode, all data used in this workwere obtained with glass-insulated microelectrodes.In the absence of stereotaxic measurement, the length and

width of the visible right optic tectum were carefully notedfor each fish. Different penetrations were made with thesame microelectrode, which was advanced with a micro-drive. The position of the electrode on the tectal surface wasalways monitored under visual control. The location of eachstimulation site in the anteroposterior and mediolateral axeswas noted with respect to the previous measurements of thetectal surface. Among the goldfish used here, the tectal sizevaried slightly (less than 5%), so we pooled data from thedifferent animals, without any form of normalization, tocompare the modification in the horizontal and verticalcomponents of the movement versus the distance from therostral pole or midline across fish (see Fig. 3). All data inthis paper are from stimulation sites on the visible rightoptic tectum. Sometimes, to explore the presence of down-ward eye movements, the tectum was gently displaced andlateral-located microelectrode penetrations were performed.The depth of the microelectrode tip was selected using the

criterion of the minimum current intensity (threshold range10–30 µA) to evoke eye movement; it was always between350 and 450 µm, at the level of the stratum grisseum centraleor the stratum album centrale (Fig. 1). To identify thelocation of the electrode tip, a small lesion was made usinga single cathodal pulse of 6 µA lasting 15 s.Eye movements were evoked with the above-mentioned

monopolar microelectrodes using a train of cathodal pulsesdelivered through a constant-current stimulus isolation unit.To determine the ‘‘vector map’’ of eye movements or the

272 C. Salas et al.

effect of the initial eye position on the evoked movement, astandard stimulus train with the following parameters wasdelivered: train duration, 70 ms; pulse rate, 384 Hz; currentstrength,z70 µA; pulse width, 200 µs. Current strength wasadjusted for each stimulation site until the amplitude andvelocity of evoked saccades reached a plateau level (seeResults). When the experiments were to determine theeffects of stimulus parameters, current strength (range,10–320 µA), pulse rate (5–1000 Hz), train duration (10–300 ms) and pulse width (0.1–1 ms) were systematicallyvaried. Current strength was calculated by monitoringthe voltage across a 10-kÙ resistance in series with thestimulating electrode.A group of at least 10 saccades was evoked from starting

eye positions near 0) to determine the vector map, fromdifferent initial eye positions randomly selected to determinethe influence of initial eye position, or with changed stimu-lus parameters but maintained chosen initial eye position todetermine the effect of stimulus parameters. A recovery timeof 5 min was left between penetrations; the experimentalsessions lasted 3–4 h.Between 20 and 30 microelectrode penetrations were

carried out in five goldfish to determine the tectal map ofeye movements. In these animals, the influence of initial eyeposition on the trajectory of the evoked saccades wasinvestigated exhaustively only in some of the penetrations.Between two and five microelectrode penetrations were

carried out in six goldfish to study the effects of stimulusparameters on the evoked movements’ metrical properties.

Histology

At the conclusion of the experimental session, the fishwas reanesthetized (1:5000 solution of tricaine methane-sulfonate) and perfused transcardially with saline solutionfollowed by 10% formalin in phosphate buffer. The brainwas removed, frozen and cut into 50-µm sections that werestained with Neutral Red to locate the stimulation sites(Fig. 1).

Data analysis

Videotape records were analysed on a processing digitalstorage oscilloscope (Tektronix, TDS 420). The horizontaland vertical components of evoked eye saccades, as well astheir velocities, were displayed on the oscilloscope screen.The following parameters were measured: initial and finaleye positions, amplitude, peak velocity and latency ofhorizontal and vertical components of saccades. To repre-sent evoked saccades as vectors, the horizontal and verticalcomponents of eye movements were transposed to an X–Ycoordinate system. In this, O) horizontal and vertical corre-sponded to the center of the oculomotor range. Tectalvector maps were obtained by representing the amplitudesand directions, in X–Y coordinates, of the characteristicvectors evoked from different stimulation sites. Each char-acteristic vector was obtained as the average of 10 move-ments evoked from the same tectal site when the eye was inthe center of the orbit (range,&2)). To determine the effectsof initial eye position on (i) the trajectories and (ii) theamplitude of evoked saccades, we plotted the position of theeye every 5 ms, in X–Y coordinates, and the amplitude ofmovements against the starting eye position, respectively.To test the influence of stimulus parameters on the evokedsaccades, each value of the stimulus parameters was applied10 times when the eye was at the same position in the orbit.Figures 2–7 show the time-course and trajectories of evokedmovement in the left eye following electrical stimulation ofthe right tectum obtained from the same representativesingle goldfish. For all figures, upward deflections indicaterightward or upward movements.

RESULTS

Tectal map of eye movement vectors: general remarks

Electrical microstimulation of the intermediate anddeep tectal layers in goldfish evoked saccadic eyemovements that maintained their final positions forseveral hundred milliseconds, except when eye con-vergence was elicited (see below). The direction andamplitude of the characteristic vectors depended onthe stimulated site (Fig. 2). Thus, we found a changein the direction of eye saccades from upward todownward when the stimulus was displaced in themediolateral axis of the tectum (Fig. 3A–D). Inaddition, there was an increase in the amplitude ofthe horizontal component of saccades when thestimulus was moved in the anteroposterior direction(Fig. 3E–H). Variations in the characteristic vectordirection with the distance to the midline were wellfitted by linear regressions for all five goldfish inwhich the tectal vector map was studied (range ofcorrelation coefficients=0.88–0.96; also see Fig. 3C).These linear relationships were determined for each

Fig. 1. Photomicrographs of a transverse section to showthe stimulus site location. (A) Mesencephalic transversesection to show the location of stimulation sites (arrow-heads) on a low-magnification view of the goldfish tectum.(B) Photomicrograph of the area outlined in A to showmore precisely the location of the electrolytic markinglesion. OT, optic tectum; SAC, stratum album centrale;SFGS, stratum fibrosum et griseum superficiale; SGC,stratum griseum centrale; SM, stratum marginale; SO,stratum opticum; SPV, stratum periventriculare; TL, toruslongitudinalis; TS, torus semicircularis; VCb, valvula

cerebelli; IV, trochlear nucleus.

Tectum and eye movements in goldfish 273

animal from stimulating sites in the same coordinatesas those of Fig. 3A. The slopes of the linear regres-sion lines (range=3.75–7.51) were not different(Student t-test, P§0.95). The amplitude of the hori-zontal component of saccades also increased withdistance from the rostral pole of the tectum. Again,well-fitted linear relations for all five goldfish werefound (range of correlation coefficients=0.68–0.85;see Fig. 3G). However, the correlation coefficientswere lower in these relationships than in those foundfor the mediolateral axis, because the horizontalcomponent amplitudes of eye movements becamesaturated by the middle of the tectum, with nofurther increase with caudal displacement. In ad-

dition, linear regression lines (slope range=1.72–3.05)were not different between fish (Student t-test,P§0.95).Some peculiarities may be observed in the tectal

map of characteristic vectors. First, the change indirection of the vertical eye component from up-ward to downward did not occur at the sametransverse tectal level (Figs 2, 3A, B). Second, purevertical eye movements were never elicited. Third,together with the tendency of the horizontal compo-nent amplitude to increase, the upward componentof movement decreased when the stimulus wasmoved from anterior to posterior in the tectum(Fig. 3E, F). The decrement in the vertical compo-

Fig. 2. Representation of the characteristic vectors of evoked saccades depending on the stimulation sitein the right tectum for a single representative goldfish. Each characteristic vector represents the directionand amplitude average of 10 electrically evoked movements. The drawing also illustrates the location ofthe different functional tectal zones distinguished in this work. At the top right is shown a dorsal viewof the goldfish’s brain, in which the boxed area indicates the location of the tectum as well as the regionof the brain enlarged in the main drawing. Cb, cerebellum; OT, optic tectum; Tel, telencephalon; VL,vagal lobe; c and u indicate contraversive and upward directions of evoked saccades, respectively.

Calibrations are as indicated.

Fig. 3. Changes in direction and amplitude of electrically evoked saccades depending on the stimulatedtectal site. (A) Location of four different sites (1–4) in the mediolateral axis. (B) Transverse sectionsshowing the directions and amplitudes of the characteristic saccadic vectors evoked following electricalstimulation of the tectal sites indicated in A for a single representative goldfish. Note that the evokedsaccades changed the direction, from upward to downward, when the stimulation site was displaced inmediolateral tectal axis. (C) Linear relationship of the variation in the vertical amplitude (V. Ampl.) withthe displacement of the stimulating site in the mediolateral tectal axis. Open circles indicate the verticalamplitudes obtained following each stimulation of the same tectal sites represented in B. (D) Linearrelationships, similar to C, obtained for five different goldfish. (E) Location of seven tectal sites (1–7) inthe anteroposterior tectal axis. (F) Parasagittal drawing of the tectum showing the characteristic saccadicvectors evoked following the stimulation of sites illustrated in E for a representative goldfish. Note boththe increase of the horizontal component of the evoked saccade and the flattening of the movements whenthe stimulation site was displaced in the tectal anteroposterior axis. (G) Linear relationship showing theincrease of the horizontal component amplitude (H. Ampl.) of the evoked movements represented in F.Open circles indicate amplitudes obtained following each stimulation of the same sites represented in F.(H) Linear relationships similar to G obtained for five different goldfish. CCb, corpus cerebelli; VCb,valvula cerebelli; d and i indicate downward and ipsiversive directions of evoked saccades, respectively.

Other abbreviations are as in Fig. 2. Calibrations are as indicated.

274 C. Salas et al.

nent along the anteroposterior axis was fitted by alinear regression (range of correlation coefficients=0.61–0.86); this tendency was present in all the fivegoldfish (slope range="0.31 to "3.17). Finally, asshown in Fig. 2, the topographical representation of

small eye saccade sizes on the tectum is not asmagnified as reported in monkeys.47

Dependence of evoked saccades on either thestimulation site, the influence of the initial position ofthe eye in the orbit or the effects of long train

Fig. 3

Tectum and eye movements in goldfish 275

stimulation enabled four functional zones to bedistinguished, which are defined following theiranatomical locations on the tectum (Fig. 2).

Tectal map of eye movements: functional zones

The medial zone occupies the largest area of thetectum (Figs 2, 4A). Stimulation of this zone alwaysevoked contraversive saccades with upward ordownward vertical components, whose directionand amplitude depended on the tectal loci (Fig 2,4B). From any stimulation site in this zone, evokedsaccades had trajectories which where roughlyparallel and had similar amplitudes (Fig. 4A–C),

regardless of initial position. For examples a and bof Fig. 4B, the correlation coefficients, for therelationship between saccade amplitude and initialposition, were 0.71 and 0.80; the regression slopeswere 0.28 and 0.23, suggesting little dependence ofsaccade amplitude on initial position. These valueswere lower than those of the anteromedial zone(see below). Stimulus trains lasting between 100 and300 ms were applied in different sites of thismedial zone. From all of the studied sites, this longstimulation evoked a staircase of two or threesaccades, which drove the eyes to the extremeof the oculomotor range (Fig. 4D). Stimu-lation of this zone evoked conjugated movements

Fig. 4. Time-course and trajectories of eye saccades evoked from two representative tectal sites (a, b) of themedial zone in a single animal. (A) Location of stimulus sites on the dorsal surface of the tectum. (B) Thetime-course of five (1–5) evoked saccades from different initial eye positions in the horizontal plane. (C)Trajectories of the movements illustrated in B. (D) An example of the staircase of saccades evoked whendifferent sites in the medial tectal zones were stimulated with a long-lasting stimulus train. Arrows denotethe start of a saccade and arrowheads the peak of velocity. Cb, cerebellum; TC, tectal commissure; Tel,telencephalon; Eh 0, Ev 0, horizontal and vertical central positions of the eye in the orbit; Eh, Ev,horizontal and vertical components of eye positions; E~ , eye velocity trace; Stim, stimulus; U, D, C and I,upward, downward, contraversive and ipsiversive directions of eye movements, respectively. Calibrations

are as indicated.

276 C. Salas et al.

of both eyes with similar amplitudes (never morethan 3) of difference in the horizontal andvertical planes) and latencies (30.7&2.5 and33.1&2.77 ms for contralateral and ipsilateral eyes,respectively).The anteromedial zone occupies the rostral and

medial areas of the tectum (Figs 2, 5A). The stimu-lation of this zone evoked goal-directed movements(Fig. 5B, C). These movements led the eye to aparticular region within the oculomotor range,which varied depending on the stimulated tectal site.Elicited saccades showed an upward component andcontraversive or ipsiversive horizontal displacements,depending on the initial eye position (Fig. 5B, C).

Another characteristic of these saccades was thattheir trajectories were often curved (Fig. 5C). Thelatencies of contraversive eye saccades were usuallyshorter (33.1&7.88 ms) than the ipsiversive ones(57.3&5.34 ms), although in certain cases the differ-ence was not more than 5 ms (see example a in Fig.5B). The amplitude of these movements depended onthe initial position of the eye in the orbit (Fig. 5D;correlation coefficients=0.97 and 0.96; slopes forthese relationships=0.83 and 0.46). When stimulustrains lasting between 100 and 300 ms were applied tothis tectal zone, the eye reached the goal and stayedthere while stimulation continued, i.e. a staircase ofsaccades was not evoked.

Fig. 5. Time-course and trajectories of eye saccades evoked from two representative tectal sites (a, b) of theanteromedial zone in a single goldfish. (A) Location of stimulus sites on the dorsal surface of the tectum.(B) The time-course of five (1–5) evoked saccades from different initial eye positions in the horizontalplane. (C) Trajectories of the movements illustrated in B. (D) Plot of horizontal component of amplitude(ordinate) versus initial eye position (abscissa). Solid lines are least-squares linear regression for theevoked saccades from stimulation sites a (triangles) and b (filled circles). The equations for the dataobtained from the stimulation sites a and b respectively are: horizontal amplitude=0.6+0.83IEh,regression coefficient, r=0.97; horizontal amplitude=4.4+0.46IEh, r=0.96. IEh, initial position of the eye

in the horizontal plane. Other abbreviations are as in Fig. 4. Calibrations are as indicated.

Tectum and eye movements in goldfish 277

The extreme anteromedial zone occupies a narrowstrip lying within the rostral pole of the tectum nearthe tectal commissure (Figs 2, 6A). Stimulation ofthis area evoked convergent eye saccades (Fig. 6A–C), i.e. from every initial position of the eyes in theorbit, the eye contralateral to the stimulated tectum

showed ipsiversive movements and the ipsilateral eyecontraversive movements (Fig. 6E). Stimulationdrove both eyes nasally to the extreme of the orbit,but when the stimulation ended, the eyes quicklyreturned to a nearly original position (Fig. 6B). Thevelocity of the nasal movements was significantly

Fig. 6

278 C. Salas et al.

higher (538&84.97 )/s) than the returning one(330&44.72 )/s). Therefore, in contrast to any othertectal zone in this extreme anteromedial zone, it wasnecessary to deliver a long-duration stimulus, usuallylonger than 100 ms, to maintain the final position ofthe eyes after saccades (Fig. 6E). In the convergentmovements the upward components were almostabsent (never more than 2); Fig. 6B, C). Figure 6C, Dshows that the amplitude of the horizontal compo-nent of the nasally directed saccades exhibited alinear relationship with the initial position of the eyein the orbit (correlation coefficients=0.94 and 0.97;slopes of these relationships=0.91 and 0.74). Theslopes of these relationships denote a strong influenceof initial eye position on the amplitude of evokedsaccades. The amplitude of movements of both eyeswas largely unequal in reaching the same extremenasal position during evoked convergence (Fig. 6E)and was dependent upon the initial position of eacheye. Saccades of both eyes started with similar laten-cies (13.3&2.5 and 15.6&2.88 ms for contralateraland ipsilateral eyes, respectively).The posterior zone is located in the caudal tectum

(Figs 2, 7A). Stimulation in this zone evoked eyemovements with little, if any, upward component(even when evoked from its medial part; Fig. 7B, C)and vigorous tail movements. As in the medial zone,all saccades were contraversive but, in distinctionto the medial zone, the amplitude of the posteriorzone saccades was linearly dependent on the initialposition of the eyes in the orbit (correlationcoefficients=0.98–0.95; regression slopes=0.71–0.79).Long-lasting stimulus trains (100 ms) evoked a stair-case of two or three saccades (Fig. 7D). Thesesaccades were coupled in both eyes, showing similarlatencies (41.1&2.47 and 45.5&3.12 ms for contra-lateral and ipsilateral eyes, respectively) andamplitudes.

Dependence of electrically evoked saccade metrics onstimulus parameters

The effects of stimulus parameters on saccadefeatures were observed qualitatively at 15 sites of

different zones. From any site in the above-mentioned tectal zones, the amplitude, velocity andduration of evoked saccades were dependent onvariations in current strength, pulse rate or durationof stimulus train. However, the direction of move-ments remained unaffected by modifications in suchparameters.The quantitative effects of stimulation parameters

on evoked saccades were determined at four siteswithin the medial zone of different animals. Figures 8and 9 illustrate a representative example of thequantitative effects of stimulation parameters on sac-cades evoked from a single site within the medialzone. Changes in the parameters of current strengthand pulse rate influenced the evoked saccades in asimilar way (Fig. 8). Thus, for a stimulus train ofconstant duration (70 ms) and pulse rate (384 Hz),the increase of current strength from 10 µA (usuallythe threshold level to evoke eye saccades) to 70 µAled to a notable increase in the amplitude and peakvelocity of evoked movements (Fig. 8A). When cur-rent strength exceeded 70–100 µA, amplitude andpeak velocity of evoked saccades reached plateaulevels. Increases in current strength had only a smalleffect on the duration of saccades, and no effect onthe direction of the saccade vector (Fig. 8A). On theother hand, latencies of saccade initiation decreasedfrom 64&3.4 to 29.7&2.2 ms with the increase ofcurrent strength (not shown).When stimulus train duration (70 ms) and current

strength (70 µA) remained fixed but pulse rate wasmodified from 10 to 350 Hz, a marked and gradedincrease in amplitude and peak velocity of evokedsaccades was obtained. Once the stimulus pulse rateexceeded 350 Hz, the amplitude and peak velocity ofevoked eye saccades reached plateau levels (Fig. 8B).As indicated for the effects of variations in currentstrength, changes in pulse rate scarcely affected theduration of evoked eye saccades or the direction ofsuch movements. Increases in pulse rate shortenedthe onset of evoked saccades from 72&5.1 to31.2&2.3 ms (Fig. 8B). Although amplitude andpeak velocities of saccades were modified as a func-tion of the current strength and pulse rate, the

Fig. 6. Time-course and trajectories of eye saccades evoked from two representative tectal sites (a, b) of theextreme anteromedial zone in a single goldfish. (A) Location of stimulus sites on the dorsal surface of thetectum. (B) The time-course of four (1–4) and three (1–3) evoked saccades in the left eye from differentinitial eye positions in the horizontal plane. It must be remarked that the differences in the course of thehorizontal component of eye position between examples elicited from the stimulation sites a and b werenot due to the tectal loci but to the duration of the stimulus, i.e. in this zone, the eye position followingevoked saccades was maintained only during stimulations. (C) Trajectories of the movements illustratedin B. Only the nasal component of these movements is represented. Arrowheads indicate the initial eyeposition of examples 1 and 2 of the movement shown in B part b, whose trajectories coincide with that ofexample 3. (D) Plot of horizontal component of amplitude (ordinate) vs initial eye position (abscissa).Solid lines are least-squares linear regression for the evoked saccades from stimulation sites a (triangles)and b (filled circles). The equations for the data obtained from stimulation sites a and b respectively are:horizontal amplitude="11.3+0.91IEh, r=0.94; horizontal amplitude="13.2+0.74IEh, r=0.97. IEh, ini-tial position of the eye in the horizontal plane. (E) The drawing illustrates the locations of the eyes andtheir movements (arrows) when the stimulus (st) was applied to site a in this tectal zone. On the right areshown four examples of convergent evoked saccades. LEh, REh, left and right eye positions in the

horizontal plane. Other abbreviations are as in Fig. 4. Calibrations are as indicated.

Tectum and eye movements in goldfish 279

range of eye metrics (which the stimulus parameterscould affect) was dependent on the location of thestimulating electrode within the tectum.The effects of the modifications in stimulus dura-

tion on evoked eye movements were remarkablydifferent from those of current strength and pulserate. Thus, when current strength (70 µA) and pulserate (384 Hz) remained fixed but the train durationwas increased from 30 to 100 ms, a systematic in-crease of amplitude and duration of evoked eyesaccades was observed (Fig. 9). However, the peakvelocity of such movements remained unmodifiedonce the stimulus exceeded 50 ms. As indicated forcurrent strength and pulse rate, the train durationnever changed the direction of the evoked saccadicmovements. On the other hand, stimulus trains last-ing more than 100 ms usually led to a staircase ofsaccades, except for stimulation sites located in theanteromedial tectal zones, when the long stimulusevoked a unique saccade. With the values of stimulusparameters used in the present experiment, never

more than three successive saccades were found be-fore the eye reached the extreme of the oculomotorrange. Furthermore, when a long-lasting stimulustrain was applied, the delay between successivesaccades was 25–50 ms and, during this period, theeyes showed a slow drift in their positions.When pulse width was modified from 0.1 to 1 ms,

maintaining constant current strength (70 µA), pulserate (384 Hz) and train duration (70 ms), no signifi-cant effects were observed on amplitude, velocity anddirection of evoked saccades.

Comparison between spontaneous and electricallyevoked eye saccades

Figure 10 shows the variation of saccadic peakvelocity and duration with amplitude of spontaneousand electrically induced eye displacements from themedial zone in order to demonstrate whether thekinematic properties of both types of movementare similar. As reported previously for other

Fig. 7. Time-course and trajectories of eye saccades evoked from two representative tectal sites (a, b) of theposterior zone in a single animal. (A) Location of stimulus sites on the dorsal surface of the tectum. (B)The time-course of five (1–5) evoked saccades from different initial eye positions in the horizontal plane.(C) Trajectories of the movements 1, 3 and 5 illustrated in B. (D) Three examples of staircases of saccadesevoked from the medial zone with a long-lasting stimulus train. Arrows denote the start of a saccade and

arrowheads the peak of velocity. Abbreviations are as in Fig. 4. Calibrations are as indicated.

280 C. Salas et al.

Fig. 8. Effect of current strength and pulse rate on eye movement characteristics evoked from a single sitewithin the medial zone. (A, B) At the top is shown how eye movement amplitude and velocity increasewith current strength (A) and pulse rate (B). Other plots indicate the effects of variations in currentstrength (left) and pulse rate (right) on saccadic amplitude, peak velocity, duration and direction. Openand filled circles represent horizontal and vertical components of evoked saccades, respectively. Note thatincrease in the parameters of current strength and pulse rate both modify amplitude and peak velocityof saccades until a plateau level is reached, whereas duration and direction were scarcely influenced.To represent movement directions in X–Y coordinates, 0) is used as a pure contraversive saccade and90) as a pure upward displacement. Eh, E~h, eye position and eye velocity in the horizontal plane;

C, contraversive direction of eye movement. Calibrations are as indicated.

Tectum and eye movements in goldfish 281

vertebrates,14 spontaneous saccadic eye movementsin goldfish show a non-linear saturating relationshipbetween peak velocity and amplitude, whereas therelationship between duration and amplitude isalmost linear (Fig. 10B, C). These relationships hadthe same characteristics as those obtained by chang-ing stimulus current strength (Fig. 10D, E) or pulserate (Fig. 10F, G). With the values of stimuluscurrent strength and duration used in the presentwork, for any amplitude of the saccades evokedchanging the pulse rate, the peak velocity was similarto (although slightly lower than) those obtained forspontaneous movements. The main sequence ofmovements evoked by changing stimulus durationwas notably different to that of spontaneous saccades(Fig. 10H). Thus, peak velocity of the movementsevoked by changing stimulus duration reached anearlier saturating plateau (over approximately 10))than that of the spontaneous movements (overapproximately 17)). Moreover, the duration of theseelectrically evoked saccades increased more thanthat of the spontaneous movements (Fig. 10I). Insummary, the present data show that, at least fromsites within the medial zone, the main sequence inelectrically induced eye saccades is similar to thosefound in spontaneous movements, except whenstimulus train duration was varied. Therefore, the useof this technique can mimic, albeit with certainlimitations,4,35,59 natural neural events and can pro-vide insights into the functional role of the tectum inthe generation of saccadic movements.

DISCUSSION

Tectal topography of evoked eye movements: func-tional zones

General remarks. The present results show thatelectrical microstimulation of different tectal sites ingoldfish evoked various types of eye movement. Asdiscussed below, these data suggest the presence ofdifferent tectal functional zones, which might revealtectal mechanisms particular to this species besidesthose in common with other vertebrate groups. In

Fig. 9. Effect of stimulus duration on eye movement char-acteristics evoked from a single site within the medial zone.At the top is shown how eye movement amplitude increaseswith stimulus duration, whereas the peak velocity of sac-cades remains almost unaffected with stimuli lasting morethan 50 ms. Other plots indicate the effects of variation instimulus train duration on saccadic amplitude, peak vel-ocity, duration and direction. Open and filled circles indi-cate horizontal and vertical components of evoked saccades,respectively. Note that increases in stimulus duration lead torises in amplitude, duration and peak velocity of saccades,but this latter characteristic reaches a plateau level beforethe others. To represent movement directions in X–Y co-ordinates, 0) is used as a pure contraversive saccade and 90)as a pure upward displacement. Eh, E~h, eye position andeye velocity in the horizontal plane; C, contraversivedirection of eye movement. Calibrations are as indicated.

282 C. Salas et al.

fact, some of these adaptive peculiarities indicatetectal involvement, in a lateral-eyed animal such asgoldfish, not only in orienting response but also inother more complex motor tasks.

Medial tectal zone and orienting responses. It iswidely accepted that eye saccades aim to put the imageof a novel target on to the fovea and, hence, themovements are encoded tectally in accord with aretinotopic map.47 Similar to other vertebratespecies,17,32,47 electrical stimulation of the medial tectalzone in goldfish also showed a tendency to modify thedirection of eye saccades from upward to downwardwhen the stimulus was displaced in the mediolateralaxis of the tectum, and to increase the amplitude of thehorizontal component of the saccade when the stimu-lus was moved from anterior to posterior along thetectum. These variations were roughly in agreementwith the overlying retinotopic visual map.23,53,58

The present results show that long-duration pulsetrains applied anywhere within the medial tectalregion evoked a staircase of saccades. In addition, theinfluence of initial eye position was slight on bothdirection and amplitude of saccades. In mammals,these results have been interpreted in favor of codifi-cation of movements on the basis of the retinotopicalmap in the superior colliculus.17,20,32,47 Do these dataimply that the optic tectum is upstream of the localfeedback loop for saccade generation? Although thisis a plausible possibility, it does not necessarily ruleout the possibility that the tectum is located withinsuch a feedback circuit coding certain temporal as-pects of the movements, as recent neurophysiologicalstudies suggest.38,39,66 Nevertheless, despite the suc-cess of later studies in the interpretation of collicularactivity in the generation of the appropriate metricsof the movement, they fail to explain how staircasesaccades are generated. Assuming the sequence ofcollicular activity proposed by Munoz and Wurtz39

were present in fish, the successive saccades evokedby a long-lasting stimulus might be produced byintratectal inhibitory circuits or from the brainstempreoculomotor areas, which reset caudal tectal zonesafter each saccade.In free-swimming preparations it has been found

that stimulation applied at different sites of thismedial zone evoked body contraversive displace-ments, occasionally with upward or downward com-ponents, depending on the tectal locus.2,36 Taking thedata of eye movements together with those of bodyturning, it is possible that this zone is involved in thegeneration of spatial orienting responses in eithervertical or horizontal planes, as suggested in othervertebrates.29–31 The performance of tectally evokedorienting responses by means of synergistic move-ments of eye and head or body is widespread amongall vertebrate species studied.8,13,45,48,49,60

Anteromedial zone and goal-directed saccades.Stimuli applied to the tectal anteromedial zone ingoldfish evoked goal-directed eye movements. These

movements are characterized mainly by pronouncedeffects of the initial eye position on the trajectory,direction and amplitude of evoked saccades. Inmonkeys and cats, movements with similar featureshave been reported following electrical microstimula-tion of the posterior collicular zones.4,17,33–35,48,54 Inaddition, notable effects of initial gaze position onthe gaze-evoked saccades have been found inmonkeys,55,56 although not in cats.45

Different hypotheses have been proposed to ex-plain the neural processing in the oculomotor systemfor the generation of these goal-directed movements.McIlwain34,35 suggested that an underlying feedbackcircuit with a variable gain element might yield thesemovements. More recent proposals have pointed outthat a subgroup of superior colliculus neurons areinside the local feedback loop controlling saccadedynamics.7,18,19,27,38,39,44,66 This feedback loop pro-vides a current change in eye position and/or velocitysignal that is used to generate the appropriate motorcommand to drive the premotor pools. Therefore,while speculative, a feedback path which incorpo-rates a variable gain element might underlie thegeneration of goal-directed movements from theanteromedial zone of the goldfish tectum. This view issupported by the reported activity of some neuronscarrying an efference copy of eye movement to thetectum in fish.24,42 Such a signal could be used to feedthis hypothetical tectal comparator in the feedbackcircuit for saccade generation. The presence of goal-directed saccades in one portion of the tectum (theanteromedial zone) and not in others (e.g., the medialzone) suggests that the feedback to each of theseportions of the tectum is inherently different. Thiswould suggest that either the goal-directed move-ments result from different afferents to these portionsof the tectum, or these two regions project to differ-ent portions of the saccade generator in the brain-stem. Another possible explanation is that theintrinsic inhibitory interconnections within the tec-tum could be organized differently in each of thesevarious zones of the tectum.Other suggestions have also been attempted to

explain the presence of eye and/or head movementswhich depend on the initial position of eye and/orgaze. Segraves and Goldberg56 proposed that, duringnatural or voluntary gaze shifts, the collicular signalis adjusted by downstream oculomotor structures tocarry the appropriate motor command to ocular andneck motoneurons, i.e. taking into account thelength–tension muscle relationships as well as theelastic forces of the orbit. In this sense, it has beensuggested that the same collicular command gener-ates different movements depending on the state ofdownstream circuits. This could also imply that thecomparison between desired and real movementoccurs downstream of the superior colliculus.40

Other possibilities have also been suggested. Forexample, the goal-directed movements could be aresult of the stimulus current spread to the collicular

Tectum and eye movements in goldfish 283

Fig. 10. Comparison of spontaneous eye saccades with those evoked by electrical stimulation from a singlesite within the medial zone. (A) Time-course of the horizontal component of spontaneous eye movements(a) and those evoked by changes in stimulus parameters: current strength (b), pulse rate (c) and duration(d). Arrowheads indicate the onset of stimulus. C, contraversive direction of eye movement; Eh0,horizontal central position of the eye in the orbit; E~h, eye velocity in the horizontal plane. Calibrationsare as indicated. Variations of peak velocity and duration with the horizontal amplitude of spontaneous(B, C) and electrically evoked eye saccades following stimulus changes in either current strength (D, E),pulse rate (F, G) or duration (H, I). The star in H indicates the amplitude at which the peak velocity

reaches the saturating level.

284 C. Salas et al.

zones which code retinotopic and centering sac-cades.33 Another idea posits a saturation elementplaced between the superior colliculus and eye sac-cade burst generator, thereby providing a neuralsaturation in eye position.27,45 Because of the lack offunctional data in fish and also because thiswork does not directly address the testing of suchhypotheses, we do not have evidence which wouldparticularly favor any one of these ideas.

Extreme anteromedial tectal zone and eye conver-gence movements. As shown here, stimulation appliedto different sites within the extreme anteromedialtectal zone evoked eye convergence. This type of eyemovement has never been reported following electri-cal stimulation of the tectum in land vertebrates, butis usually present in all species of fish investi-gated.1,2,36 Unitary recordings of sensory cells withinthis zone show that their receptive visual fields extenda few degrees over the midline, within ipsilateral andcontralateral nasal sides.23,53,58 The overlapping ofthe two visual fields is probably related to sensori-motor requirements to generate eye convergencefrom the tectum. These tectally evoked movementsrepresent a particular orienting response of lateral-eyed teleost fishes, probably aimed to project anobject on both central retinas, thus giving the animalsa certain degree of depth perception. This might beuseful for solving many tasks, for example accuracywhen catching food.64,68 The hypothesis that thistectal zone could be involved in motor activities suchas food catching behavior is supported by comp-lementary data obtained in free-swimming fish. Thus,the animal performs forward movements in a ‘‘foodsearching’’ manner following the electrical stimula-tion of anterior tectal zones,2,36 and fails to pursueand catch food pellets after bilateral tectal ablation.68

Available studies have not reported eye vergenciesfollowing electrical collicular stimulation in frontal-eyed mammals.17,20,47 In addition, neither eye con-vergence32 nor movements to ‘‘search food’’43 wereobserved in lateral-eyed mammals such as rodentswhen the stimulus was applied to the colliculus. Allthese data could denote the involvement of particularadaptive tectal mechanisms for eye convergence andfood catching in fishes.

Posterior tectal zone and escape responses. Stimu-lation applied to the posterior tectal zone evokedcontraversive eye movements whose vertical compo-nent was scarce or absent. The absence of such avertical component reveals a discrepancy between theretinotopic arrangement of the tectum in its super-ficial layers23,53 and the motor properties of itsdeeper layers (present data). A possible explanationfor this result comes from studies of tectal stimula-tion in free-swimming fish, which suggest that theposterior tectal zone is specialized in the generationof escape behavior rather than in orientingresponses.2,36 Such a hypothesis is supported by

additional different evidence: (i) stimulation of thiszone in the free-swimming fish evokes flight reactionthat includes a sudden halting of normal activity,dorsal fin erection, backing movements at loweststimulation, rapid turning of about 180) at higheststimulation, and swimming to the edge of the tank;(ii) this is the tectal region with the lowest thresholdfor evocation of body movements, and when it isstimulated, the animal performs body turning exclu-sively in the horizontal plane. The suggestion that thecaudal pole of the tectum, or the immediately under-lying structures, is involved in flight reaction mightalso be inferred from studies in other vertebrategroups.43,49 In summary, the horizontal eye move-ments evoked from goldfish’s caudal tectum might bea component of a more complex motor response thatincludes body turning in the horizontal plane duringthe escape responses.12,41

Dependence of eye movement characteristics onstimulus parameters

Early reports suggested that the superior colliculusevoked eye movements whose direction, amplitudeand velocity were topographically encoded.47 Never-theless, recent evidence reveals that although thestimulated site within the tectum yields the directionof movement, its metrical characteristics are corre-lated with stimulus parameters. Indeed, graded rela-tionships between tectal stimulation parameters andeye,17,59,65 gaze,45 head8 and body25,43 displacementshave been established. Data reported here show thatthe dependence of saccade features on stimulus par-ameters are also present in teleost fishes. Thus, thecodification of eye movement metrics by means ofchanges in the level of activity in the tectum (asmanipulated by stimulus parameters) seems to be amechanism largely conserved across vertebrates.The relationships between stimulus parameters and

evoked saccades in goldfish suggest that direction,velocity and duration of saccades might be encodedin different aspects of the tectal activity. Thus, theeffects of increasing current strength and pulse rateon saccade features were similar. They led to anincrease of amplitude and peak velocity of saccadesuntil reaching a plateau level; otherwise, the directionand duration of movements remained almost un-changed. As already suggested by others,45,59,65 thelevel of electrically induced tectal activation is relatedto the velocity and amplitude of evoked saccades byaffecting the discharge rate of activated cells and/orthe size of activated population. The influence ofthe level of tectal activity on saccade velocitymight also be inferred from different studies inmammals.3,22,26,38 Thus, the activity profile of somecollicular neurons co-varies with the instantaneouseye velocity during saccades,3,38 and the pharmaco-logical treatment of small regions of the colliculusleads to changes in saccade velocity but not inamplitude.22,26

Tectum and eye movements in goldfish 285

Although changes in stimulus parameters modifiedsaccade metric properties, the influence on thedirection of the movements was almost nil. Increasesin current strength and frequency led to proportionalchanges of both horizontal and vertical componentsof evoked movements. The absence of effectsof changing stimulus parameters on movementdirection has also been reported in other verte-brates.8,45,59,65 As already suggested,59 the absence ofmodification in saccadic direction might be based onthe fact that the same tectal locus (and perhaps thesame collicular cells) project to both premotor verti-cal and horizontal pools of the oculomotor system37

and, hence, the variation in the level of tectal activityaffects both brainstem generators equally. Thus, theunchanged direction of evoked saccades in goldfishcould be the result of a similar underlying tectalefferent organization.61

Increases of stimulus train duration led to increasesin amplitude, velocity and duration of the evokedsaccades, until all these variables reached theirplateau level. However, saccade velocity reached itsplateau level with shorter stimulus than the othervariables. Similar results were reported in monkeys,59

cats45 and owls8 measuring eye, gaze and head move-ment characteristics, respectively. It has been sug-gested that the movements elicited by changingstimulus train duration seem to be saccades whosetrajectories were truncated45 and unnatural.8 Indeed,such movements are certainly unnatural because theamplitude versus velocity relationship is differentfrom that observed with spontaneous saccades (Fig.10H). Nevertheless, the current results suggest thatthe size and duration of a saccade might be related toduration of the activity in a particular tectal locusand, furthermore, that velocity and amplitude ofsaccade might be encoded in different aspects of thetectal activity. The presence of such independentsignals in mammals would explain, for instance, whysome drugs applied to the superior colliculus modifythe velocity of movement without affecting itssize.22,26

In summary, all the results shown here might implythat not only the locus but also the level and durationof tectal activity are important for the downstreamoculomotor circuits to generate a saccadic move-ment. A similar conclusion has been arrived at inmonkeys.59,65 As already stated,59 these findings haveimportant implications for the current view of therole of the superior colliculus in the generation of eyesaccades, and are incompatible with the major as-sumption of earlier studies that posited that thesite of collicular activity alone encodes the desireddisplacement. Indeed, the modification of saccade

metric properties by means of changes in tectalactivity is in accord with recent data showing thatthe firing rate of some collicular neurons might betemporally encoding some movement features.38,39,66

Furthermore, the present data invite the suggestionthat collicular activity could independently encodethe velocity and amplitude of the movement. Suchideas will need to be incorporated in future models ofthe saccadic system.

CONCLUSIONS

The present results are complementary to thosereported in free-swimming fish following electricalstimulation, and suggest the presence of differenttectal zones that might be related not only to orient-ing responses, but also to other more complex motortasks. Stimulation in the tectal extreme anteromedialzone elicits convergent eye movements and is prob-ably involved in feeding behavior, namely in thelocation and catching of food. Stimulation in themedial zone drives eye movements in accord with aretinotopic representation, and could participate inthe performance of eye- and body-orienting displace-ments. Electrical stimulation of the tectal posteriorzone evokes large horizontal eye movements andcould be adaptively organized to generate a reper-toire of flight responses. The presence of these func-tional tectal zones could reveal adaptive speciesdifferences in the functional role of this structure ascompared with other vertebrates.The present results also show that evoked eye

saccade features depend on the tectal site of stimula-tion, the stimulus parameters and, in some zones, onthe initial eye position. Thus, the tectal locus encodesthe direction of the movement, whereas the metricproperties of the saccades are determined by both thestimulated locus, and the level and duration of tectalactivity. Similar results have been reported previouslyfor other vertebrate groups, and this suggests thattectal mechanisms underlying the generation ofthese movements are highly conserved across thephylogeny of vertebrates.

Acknowledgements—We wish to thank Drs D. Guitton, O.Hardy, E. I. Knudsen and C. Thinus-Blanc for their helpfulsuggestions and critical reading of a previous version of themanuscript. We greatly appreciate the kindness of Dr T. R.Stanford for sending us a preprint about the dependence ofeye movements on stimulus parameters in monkeys. We arealso in debt to the anonymous referees whose criticismsimproved this manuscript. We thank S. Fernandez for hercollaboration in the preparation of some figures. This workwas supported by grants DGICYT no. PB-93-0916, AccionIntegrada H-F and the Junta de Andalucıa.

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(Accepted 22 October 1996)

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