visually elicited turning behavior in rana pipiens: comparative organization and neural control of...

J Comp Physiol A (1996) 178:293-305 �9 Springer-Verlag 1996

J. Roche King �9 C. M. Comer

Visually elicited turning behavior in Rana pipiens: comparative organization and neural control of escape and prey capture

Accepted: 15 August 1995

Abstract High-speed videography was used to describe the initial turning movement of visually triggered escape in frogs and to compare it with the initial turn of frog prey capture behavior. These two types of turning had some general similarities, e.g. turn duration and peak velocity were positively correlated with turn angle. However, there were kinematic differences: for turns of a given angular amplitude, escape turns consistently demonstrated shorter duration and higher peak velocity than prey capture turns. There also were differences in spatial accuracy: prey capture turn angles were predictably matched to stimulus angles; escape turn angles were more variably related to stimulus angles. Both turning movements are believed to depend upon the optic tectum. However, given the observed differences in kinematics and spatial organization, we used lesion experiments to determine if distinct tectal efferent pathways subserve turning under each circum- stance. Large unilateral lesions of the brainstem simul- taneously disrupted both types of turning. However, smaller laterally placed lesions disrupted escape turning without disrupting prey capture turns. The kinematic differences in combination with the lesion results support the idea that the post-tectal circuitry for visually elicited turning movements is based upon separate descending pathways that control turning toward prey and turning away from threat.

Key words Frog �9 Tectum �9 Brainstem �9 Approach �9 Avoidance

Abbreviations CG central gray �9 OT optic tectum �9 SEM standard error of the mean

J. Roche King. C. M. Comer ([~) Neuroscience Group, Department of Biological Sciences, University of Illinois at Chicago, 845 West Taylor, Chicago, IL 60607, USA

Introduction

Orienting movements have long been a model system for studying sensorimotor integration in the brains of vertebrates. Novel visual stimuli elicit stereotyped movements of the eyes or coordinated eye/head or head/body movements. These orientation movements may be directed either toward (Ewert et al. 1983; Wurtz and Albano 1986; Sparks 1986) or away from (Ellard and Goodale 1988; Ingle and Hoff 1990; Corbas and Arbib 1992; Liaw and Arbib 1993) the stimuli that elicit movement.

A unifying principle in understanding the neural control of vertebrate orienting behavior is that orientation both toward and away from stimuli has been associated with the function of a midbrain structure, the optic tectum. The optic tectum receives a direct retinal projection that forms a map of visual space on the surface of both tectal lobes. Electrical stimulation of one lobe can produce both contraversive turning movements that resemble approach responses, and ipsiversive turning movements that resemble escape or avoidance (Dean et al. 1986; Ellard and Goodale 1986; Sahibzada et al. 1986; Northmore et al. 1988). Further- more, complete removal of the tectum abolishes both types of visual orienting responses (Schneider 1969; Ingle 1973; Milner et al. 1984; Ellard and Goodale 1988).

A fundamental question that remains to be answered is whether one tectofugal mechanism subserves all orienting movements. There are a number of tectal efferent pathways to the brainstem and spinal cord, and evidence in rodents has suggested that orienting "toward" and "away" may be mediated by different tectal efferent pathways (Dean et al. 1989). We have addressed this question using a tractable set of orienting movements that are characteristic of the frog, Rana pipiens.

Frogs and toads respond quickly and accurately to small moving objects by turning the head and the body

294 J. Roche King, C. M. Comer: Visuomotor organization of frog escape

toward such stimuli (Ingle 1983; Grobstein et al. 1983; Ewert 1974, 1984). This component of prey capture is a well defined, spatially organized behavior: turning angles closely match the position of stimuli (e.g. Kostyk and Grobstein 1982), as would be expected for a behavior that is target-oriented. It was previously known that frogs will respond to large looming objects by turning away from the object and jumping (Ingle and Hoff 1990). However, analysis of the specific relationship between stimulus position and a frog's motor output has not been made before. Spatial accuracy might be less evident in this response because there is no specific target for the motor output. One goal of this research was to characterize the spatial organization of visually elicited escape behavior by comparison to prey capture behavior in Rana pipiens.

Common features of neural control suggest that the turning component of prey capture and escape behavior could represent the same motor output. From studies in which retino-tectal relationships were altered (optic axons directed to the ipsilateral rather than contralateral tectum), there is convincing evidence that the tectal representation of the visual world ultimately determines the spatial orientation of turning for both escape and prey capture (Ingle 1973). Consistent with this, we have observed that complete removal of one tectal lobe completely abolished not only turning toward prey stimuli in the contralateral monocular visual field (cf. Kostyk and Grobstein 1987), but also escape turning away from looming stimuli presented in the same region of the visual field (Roche King and Comer, unpublished data).

Lesion studies have demonstrated that each tectal lobe gives rise to a crossed descending pathway for turning toward prey. Unilateral lesions of the tegmen- turn can abolish turning toward prey items in the ipsilateral visual hemifield (Kostyk and Grobstein 1987; Masino and Grobstein 1989). Therefore, another goal of this research was to determine if tegmental lesions would have the same effects on escape turning as they do on prey capture turning.

Here we describe quantitative behavioral data which indicate that the orienting movements of prey capture and escape have different kinematic characteristics. In addition, we tested the hypothesis that turning toward prey and turning away from threat depend upon distinct tectal efferent pathways. Analysis of the turning behavior of animals with lesions of tectal efferent pathways is consistent with this hypothesis. Portions of this research have appeared previously in abstract form (Roche and Comer 1993).

Materials and methods

Animals

Northern leopard frogs (Rana pipiens), purchased from commercial suppliers, were used for all experiments. Animals were maintained

on a 12 h light/12 h dark cycle in aquaria that provided both a dry and a wet surface. Frogs were fed a varied diet of mealworms, crickets, and cockroaches 2 3 times per week. Animals that were highly responsive in both prey capture and escape testing were selected for experimental use.

Data from a total of 28 frogs will be presented. Thirteen animals provided data on the kinematics of escape and prey capture turning. Fifteen separate animals provided data on the spatial organization of each type of turning. Six animals from this second group also were used in lesion studies.

Behavior

All behavior trials took place in a large, round arena (approximately 3800 cm 2, with walls 36 cm high). The inside of the arena was uniformly white. A high-speed video camera (Xybion SVC-10) was mounted directly above the arena and trials were recorded on video tape with a Sony VO-5800 record/playback deck. The system was operated at a rate of 60 pictures per second.

For escape trials, a frog was placed inside the arena and allowed to acclimate for 5 10 min. Escape responses usually were elicited by a standard "looming" stimulus. A 6 x 8 cm black square mounted on a stick was moved toward the frog from various angles around its body. With this hand-held stimulus, velocity could not be precisely controlled. However, as in studies by others (e.g., Ewert 1984; Ingle and Hoff 1990), we found that simple stimulus characteristics could be defined that led to reliable behavioral responses: On a given trial, the card was placed approximately 45 cm from the frog and moved directly toward it at approximately 350~00 cm/s (on a collision course). If no response occurred, the card was stopped just before making contact with the frog. This stimulus was presented 15 18 times per testing session and any one animal was subjected to a maximum of 2 testing sessions per day. A minimum of 1 minute was allowed between each stimulus trial in order to avoid habitu- ation.

For prey capture trials, we usually used an apparatus similar to that used for visual perimetry by Comer and Grobstein (1981), Kostyk and Grobstein (1987) and Masino and Grobstein (1989). Briefly, a clear, Plexiglas cylinder (12 cm in diameter) was placed in the center of the arena. Twelve clear plastic cups were fastened around the outside of the cylinder directly abutting the substrate. Each cup subtended approximately 30 ~ of visual angle. A frog was placed inside the cylinder and allowed to acclimate for 2 min. Dur- ing this period, the frog was fed a mealworm. The cylinder was positioned so that the frog sat with its head directly in the center, and on each trial a mealworm was placed in a cup. Thus the distance from the frog's eye to the prey stimulus was 6-7 cm. During each session, worms were placed into each of the 12 cups (corresponding to 12 visual field locations) in a random fashion. On some trials, worms were placed into cups fastened onto the cylinder approximately 10 cm off the floor of the arena. This allowed sampling of the upper visual field. Animals were fed a second worm immediately after the testing session. Subjects received no more than two testing sessions (24-30 total trials) per day.

The stimuli described above were used on most trials and were chosen for their visual salience, and because they have been used in previous work on escape and prey capture (Ewert 1974, 1984; Grob- stein et al. 1983; Ingle and Hoff 1990). Nonetheless they are complex: for example, the card might have a wind or acoustic component, the mealworms might have an acoustic or olfactory component. To be sure that purely visual stimuli would elicit the same behaviors, some trials were run in which the stimuli were patterns presented on a high contrast computer monitor. This monitor was built into the wall of the arena and presented a white screen of about the same brightness as the wall of the arena. Programs written in our lab (by F. Yeung) allowed presentation of two types of stimuli: a black square that expanded rapidly and filled the screen to mimic a looming stimulus, and a black horizontal bar (3 cm in length) that either

J. Roche King, C. M. Comer: Visuomotor organization of frog escape 295

a) remained stationary but wiggled at one end, or b) moved horizon- tally across the screen at two fixed velocities.

The efficacy of various computer generated stimuli was not directly relevant to the questions being posed here. Detailed analysis of visual stimulus parameters will be presented elsewhere (King and Comer, in preparation). The main point we wished to test (see results) was whether purely visual stimuli would be effective at eliciting both prey capture and escape. [Responses to computer generated stimuli are shown with separate symbols in Figs. 5, 6 and 8.]

Analysis

Individual turns were reconstructed by tracing the animal's initial position on the video playback monitor and then tracing over the animal's position on subsequent frames. We measured the amount of rotation between frames and the total duration of turning. To derive an estimate of peak rotational velocity, we took the maximum angular excursion between single frames and converted it to degrees per second. Since the sampling bin was almost 17 ms in duration (see above), this method may underestimate the true peak velocity. Finally, because there were some differences in motor performance, depending on the angular amplitude of an orienting response (see Results), small amplitude turns (0 ~ to 89 ~ and large amplitude turns (90 ~ to 180 ~ ) were analyzed separately in some of the figures below.

Response parameters were measured from "frame-by-frame" analysis of videotapes. When paused, our deck displays one non-interlaced video field. The system captured 60 of these per second: the duration of exposure for each visual sample (determined by the shutter speed used) was 1 ms.; the time interval between successive fields was 16.6 ms.

To measure stimulus positions, cross-hairs were used; one hair was placed on the long axis of the frog's body. For prey capture trials, the second hair ran from the center of the worm stimulus to the point on the frog's head directly between its eyes. For escape trials, the second hair passed through the center of the black card and projected toward the frog along the axis of the card's movement. The angle formed by the cross-hairs passing through either the mealworm or the card and that defining the long axis of the body was taken as the angle of stimulus. For orientation toward prey, a stimulus position directly rostral to the frog's snout represented 0 ~ and one directly caudal represented 180 ~ On escape trials, a stimulus position directly rostral to the frog's snout represented 180 ~ and directly caudal represented 0 ~ (see Fig. 7). These schemes for measuring angles are consistent with those used in previous work on prey capture and escape in a variety of animals. In particular, these conventions lead to regularities in the description of both behaviors: if animals turn directly toward a prey stimulus or directly away from an escape stimulus, then the turn angle will be exactly equal to the stimulus angle. Furthermore, on a Car- tesian graph of stimulus versus response: turns toward stimuli are plotted as points in the lower left and upper right quadrants, whereas turns away from stimuli are plotted in the upper left and lower right quadrants (Fig. 7).

In the escape response, frogs typically turn away and then leap. On playback, the tape was advanced until the frog had completed its rotation and had begun leaping. Cross-hairs were used again: one was placed to mark the frog's long body axis in its initial position, a second was placed along the body axis on the frame just before the frog's feet left the substrate. The angle between the cross-hairs was taken as the angle of initial turn.

During orientation toward prey, frogs often responded with a turn and then paused briefly before they snapped. When this was the case, the tape was advanced to the point where this pause occurred, and a hair was placed along the body axis. The angle between this hair and that corresponding to the frog's initial position was then measured to yield the angle of turn. If the frog turned and snapped in one uninterrupted movement (typically only for stimuli in the rostral visual field) the second hair was simply placed along the body axis on the frame showing the maximum angular excursion during the snap.

In both behavioral situations, most animals responded rapidly (within seconds) to stimulus presentation. For escape behavior, as explained above, if no movement was made when the looming stimulus was moved through its complete course, the trial was scored as "no response". Prey capture stimuli did not have a speci- fiable onset, since the time at which the mealworms began wiggling after placement in a cup could not be controlled. By comparison to previous studies of visually elicited prey capture, a worm was left in place for up to 30 s; if no movement of the frog occured during this time, the trial was scored as "no response".

Lesions

Animals were anesthetized by a dorsal lymph sac injection of 0.3~).5 cc of tricaine (1 gram/100 ml, dissolved in physiological saline). The brain was reached through the roof of the mouth. With the jaw retracted, a small incision was made in the soft palate. The palate was opened and the parasphenoid bone was scored with a scalpel to create a square opening. The level of this opening was intended to provide access to the brainstem between the obex and the entry point of the VIIIth cranial nerve. When the score lines were extended through the bone, the square was removed and kept in saline. The meninges were then opened with fine forceps. A mid-line blood vessel was used as a guide. A vacuum aspirator with a tip fabricated from a glass pipette was used to remove small amounts of tissue on either the right or left side of the mid-line blood vessel. After tissue was removed, the bone piece was placed back into position and the soft palate was pulled back to cover the area of surgery. Most animals were active within 3045 min after surgery, and fed within 24-48 h.

Postlesion data were collected between 2 and 10 days after surgery. At the completion of an experiment, animals were deeply anesthetized with tricaine and perfused through the heart with a saline/tricaine wash and then Bouin's or Karnovsky's fixative. The entire brain was then extracted for histological analysis. After post fixing for at least 24 h, brains were either dehydrated and embedded in paraffin or saturated with sucrose and prepared for frozen section- ing. Cross sections (20 or 40 ~tm thick) were stained with cresyl violet, observed microscopically and photographed. Reconstruc- tions of lesion sites were drawn from serial sections using a camera lucida.

Some animals were lesioned on the left side of the brainstem and some were lesioned on the right side. Behavioral deficits, when present, were related to the side of the lesion and no effects due to the laterality of lesions were detected. To simplify presentation of lesion effects, data from right side lesioned animals were normalized to represent the lesion as if it were on the left side.

Statistics

Averages reported here are given as the mean plus or minus the standard error of the mean. All statistical comparisons were made with tests provided in the SigmaStat software package (Jandel Scientific, San Rafael, CA). Mann-Whitney tests were used for comparing means derived from videographic analyses of behavior. Responses to computer-generated stimuli were compared with responses to more natural stimuli using one-way ANOVA. Chi square tests (2 x 2 design) were used for comparing pre- and post-lesion turn direction in experimental animals and controls. (The metric for turn direction was percent "correct" turns. For escape, contraversive turns were defined as "correct"; for prey capture, ipsiversive turns were defined as "correct".) Because lesions were made unilaterally, responses to stimuli presented in the left or right visual hemifields were analyzed separately. Linear regression was used to describe

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data from normal animals for "main sequence" analysis (Bahill and Stark 1979, see below), and to calculate a measure of spread (r 2 statistic) for plots of stimulus angles versus turn angles.

Results

Turns made away from a looming stimulus or toward a prey stimulus are similar in form and can be distin- guished most easily with the unaided eye by what they lead up to: jumping in the case of escape, and snapping at prey in the case of prey capture. High-speed videography revealed more details (Figs. 1 and 2). In turns elicited for either purpose, the animal's reorientation in space was accomplished largely by rotation of the whole body that involved movements of the limbs. (It is our impression that escape turns relied predominantly on laterally directed pushing with the two forelimbs, whereas prey orientation relied on a sequence of repositioning movements involving all four limbs. Because limb movements could not always be visualiz- ed clearly, we did not quantitate this aspect of motor behavior, but such a difference can be seen by comparing Figs. 1 and 2. This point will require further study.) Separate reorientations of the head on the body are possible, but they occurred infrequently and only when stimuli were within a restricted range. For example, deviations of the head of up to 10 degrees were some- times seen toward prey stimuli in the rostral visual field. However for responses beyond this range, virtually all of the angular deviation depended upon reorientation of the body. This is the motor component on which we have focused our analysis.

Videographic reconstructions of escape and prey orientation

In order to look for similarities as well as differences between turns made toward versus away from visual

J. Roche King, C. M. Comer: Visuomotor organization of frog escape

stimuli, we first examined reconstructions derived from "frame-by-frame" playback of responses. In several re- spects (see below), there appeared to be slight differences in turns depending upon their angular amplitude. Therefore in our initial analyses we consider small and large amplitude turns separately. Figure 3 shows representative small amplitude turning responses toward prey (panels A and B) and compares them with a typical small amplitude escape turn (panel C). On some prey capture trials, animals rapidly turned toward the prey and briefly paused before making any subsequent movement (Fig. 3A). On many trials, however, the animal's turn was continuous with a lunge and snap, as shown in Fig. 3B. This resulted in a simultaneous forward propulsion of the body. This type of continuous response often occurred for prey stimuli placed in the frontal visual field (eliciting small amplitude reorientations), but rarely for stimuli placed at more caudal locations. Figure 3C illustrates an escape response directed away from a looming stimulus. This escape turn, like the prey orientation turn in Fig. 3B, was a small amplitude turn with a forward propulsion of the body. Escape responses of small amplitude (responses to stimuli approaching from the rear) were almost always executed in a fluid fashion with the turn and jumping components superimposed. Thus in overall form they resembled the more frequently seen pattern of turning for frontally located prey stimuli. No attempt will be made here to compare the forward propulsion phase of the two behaviors.

Superficial similarities between escape and prey orienting turns also were present when larger amplitude turns were examined. Figure 4 depicts representative large amplitude escape turns (panels A and B) and compares them with a typical large amplitude prey orienting response (panel C). In contrast to small angle escape turns (Fig. 3C), this and most other large amplitude escape responses included a pure rotation phase before any forward displacement of the body began (i.e.

Fig. 1A-D Video records of a typical visually elicited escape response. Each picture is a single, non-interlaced video field. A Video field just prior to response: card approaches from front left. B Two fields (32 ms) later: animal is about half-way through a right turn. C Three fields (47 ms) after B: turn is near maximum excursion (116~ D Two video fields (32 ms) after C: leap has started


Fig. 2A-D Video records of a typical visually elicited orientation response to prey. Each picture is a single, non- interlaced video field. A Video field just prior to response. B Six video fields (99 ms) later: animal is about halfway through a right turn. C Six video fields (99 ms) after B: animal paused at this point. Total turn amplitude was 120 ~ D 25 video fields (415 ms) after C: animals is in the middle of a lunge (note tongue extension) B f C

Fig. 4A, frames 1 3). We consider it reasonable to treat the rotation phase of escape as potentially separate from the jump because on occasion pure rotation responses were elicited by looming stimuli (Fig. 4B). A typical large amplitude prey orientation response is shown in Fig. 4C. Little if any forward displacement of the body occurred during this response. As mentioned above, frogs rarely snapped directly at prey stimuli placed at such caudal locations in the visual field.

Duration and peak velocity for escape and prey capture turning

Despite some similarity of turns produced to initiate each type of orienting behavior, the timing of turn execution was consistently different depending upon whether the turn was away from a looming stimulus or toward a prey item. Escape turns typically were performed more quickly than prey capture turns of equal angular amplitude. This was evident in the responses shown earlier. In Fig. 1, a turn of approximately 100 ~ was generated between panels A and C, followed by continued turning and a jump. This turn was similar in amplitude to the turn shown in Fig. 2, between panels A and C. However, the escape turn in Fig. 1 was accomplished in 79 ms, whereas the turn toward prey of similar angular amplitude in Fig. 2 was accomplished in 198 ms.

These examples are representative of the consistent differences noted between escape and prey orientation. The mean duration for escape (95 _+ 4 ms, n = 49) was substantially shorter than the mean duration for prey capture (194 _+ 12 ms, n = 50). This difference is significant at the P < 0.001 level. An estimate of peak velocity was then calculated for each trial as described in Methods. Average peak velocity was significantly higher for escape (1309 _+ 50 deg/s) than for prey capture (775 _+ 32 deg/s). This difference was also statistically significant at the P < 0.001 level (n for each group same as above).

The reconstructions also were used to derive profiles that described the development of turning through time (from one positional sample to the next). In Fig. 5, data were pooled from 49 escape trials and 50 prey capture trials. As is evident from the figure, the metrics of movement for the two types of orienting behavior were different, and the differences were obvious for both small and large amplitude turns. In prey capture, turning proceeded at a relatively constant velocity of 6 12 ~ per unit time (16.6 ms - see Methods), compared to escape where turning first accelerated and then decel- erated. Characteristically, escape turns began with ap- parent velocites of 8 10 ~ per unit time, and then rose rapidly to twice that level before returning to their original level.

We also plotted the movement profiles for responses to computer generated visual stimuli (Fig. 5, left panel). There were no statistically significant differences between escape turns elicited by the expanding square generated with the computer, and the escape turns elicited by the hand held card. Mean peak velocity for small amplitude escape turns was 1138 _+ 47 for the hand held stimulus and 1024 + 70 for the computer generated escape stimulus (P > 0.05). For prey capture trials, the computer-generated stimulus used here was the stationary wiggling "worm" pattern described in Methods. Responses to this stimulus were indistinguishable not only from the responses to mealworm stimuli, but also to computer-generated "worm" stimuli moving at two different speeds. Mean peak velocity values (deg/s) for small amplitude turns elicited by the four types of prey capture stimuli were as follows: 660 • 39 for live meal worms, 658 _+ 29 for the stationary computer generated "worm", 692 _+ 39 for the slow horizontal moving "worm" stimulus, and 660 + 43 for the fast horizontal moving "worm". None of these values were statistically different from each other (P > 0.05). So for example, the velocity of prey capture turning was not determined by the velocity of the moving worm stimulus. However, the differences


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Fig. 3A-C Reconstruction of small amplitude turning responses. “Frame-by-frame” reconstructions from videotapes of (A) a typical prey orientation turn, (B) a prey orientation turn which included a lunge and snap, and (C) a typical escape response. In A and B, squiggly line represents position of stimulus (mealworm); in C, perpendicular lines represent stimulus (black card mounted on stick). The initial position of the frog is indicated by thick lines (1) representing the snout-vent axis and the position of forelimbs and hindlimbs. The frog’s rostra1 end is pointing upward on the page. Its position on subsequent frames is marked by thinner black lines (representing only the snout-vent axis; head movements not shown) that are numbered accordingly. Time interval between video “frames” (fields) = 16.6 ms. The animal’s position was drawn on every other field. The position of the visual stimulus and the measured angle of turn are indicated on the figure. Note that frame of reference for measuring stimulus angle differs for prey capture and escape (see Methods and Fig. 7)

between the mean peak velocity values for prey capture turning and mean peak velocity values devired from escape turn data were significantly different (P < 0.001). In short, the differences in the velocity profiles of escape and prey orientation appear to be general and not dependent upon the selection of certain triggering stimuli.

We next determined what strategy was used for pro- ducing turns of differing angular amplitude. Peak velocity and duration were positively correlated with turn amplitude during both escape turning and prey

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Fig. 4A-C Reconstruction of large amplitude turning responses.Re- constructions from videotapes of (A) a typical escape response, (B) an atypical escape response which consisted of an orientation turn only, and (C) a typical prey orientation turn. The frog’s initial position and subsequent movements are represented as in Fig. 3. The time interval between video fields is 16.6 ms. The animals position was drawn on every other frame. The position of the visual stimulus and the measured angle of turn are indicated. Note that frame of reference for measuring stimulus angle differs for prey capture and escape (see Methods and Fig. 7)

orientation. That is, for turns of increasingly larger amplitude, animals turned at a greater peak velocity and more time was required to complete the turns. Figure 6 shows two “main sequence” diagrams (Bahill and Stark 1979) plotting peak velocity versus turn amplitude (top panel) and duration versus turn amplitude (bottom panel). Regression lines were calculated for each set of data points. The equations for peak velocity were: (escape) y = 6.7x + 760 [r’ = 0.41; (prey capture) y = 3.5x + 438 [r2 = 0.51. The equations for duration were: (escape) y = 0.8x + 29 [r’ = 0.73; (prey capture) y = 1.8x + 22 [r2 = 0.83. All regression lines were significantly different from a line with a slope of zero (P < 0.001). Furthermore, the regressions for prey capture and escape turns were, in each instance, significantly different from each other (P < 0.001).

J. Roche King, C. M. Comer: V i suomoto r organiza t ion of frog escape 299

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Spatial organization of visually triggered escape and orientation toward prey

The spatially organized character of orienting behaviors typically can be seen on plots of stimulus direction versus turning angle (e.g. Fig. 7). We constructed a stimulus-response scatter plot for escape turns collected from 13 normal animals (n = 64 trials; Fig. 8, left). Rapid approach of a black square produced turning and jumping responses on 75% of all trials, and these responses typically were directed a w a y from the stimulus (78% of turns were contraversive).

Turning movements elicited by prey at various angles in both the upper and lower visual field (from 6 normal animals, n = 180 trials) are shown (Fig. 8, right) for comparison. Four of these animals also had provided data on escape. Frogs responded to mealworms on 97% of all trials and the turn angle was closely matched to the stimulus angle. Frogs were equally accurate in response to prey stimuli placed in the upper or lower visual field. Although the relationship between stimulus location and turning motor output was much more variable for escape responses than for prey orientation responses (r 2 was 0.3 and 0.9, respectively), it is evident from Fig. 8 that visually triggered escape turns were nonetheless systematically oriented in azimuth depending upon stimulus location.

Trials performed using the computer-generated "looming" and "worm" stimuli (e.g. Fig. 5) demonstrated that both types of behavior can be elicted by a purely visual stimulus. All responses to computer- generated stimuli had directional characteristics, and had duration and peak velocity values that fit well within the range for responses to live mealworms and an approaching card and were not distinguishable statistically (see Fig. 6 and 8).

Fig. 5 Plot summar iz ing the rate of tu rn ing for escape behav ior and prey capture .Both plots give angular extent of tu rn ing accomplished within each t ime bin (16.6 ms - t ime between video fields). O n left, turns of to ta l ampl i tude < 90 ~ are summarized; on right, turns t> 90 ~ Pooled da ta f rom 13 normal animals (n = 99 trials). Open

symbols = escape turns [circles = hand presented card stimulus, triangles = compute r generated looming stimulus]. Closed symbols = prey capture turns [circles = live mealworms as stimuli, triangles = compute r generated worm-l ike sitmuli]. Bars give _+ 1 SEM. In 9raph on right, dotted line for prey capture is no t shown past 166 ms, but actually cont inued for several more t ime bins

Effect of unilateral lesions on escape and prey capture turning

We have begun analysis of behavior following unilateral lesions of the tegmentum in order to determine if escape turning is affected in a similar fashion to prey capture turning. Here we will report results on six animals whose lesions have been completely reconstructed. Lesions in experimental animals were aimed at removing tissue largely in the transeverse plane, and reconstructions showed that damage was always caudal to the VIIIth nerve and restricted to a ros- trocaudal extent of 300-600 ~tm. None extended closer than 600 pm to the obex. Two of the experimental animals had large lesions that invaded the brainstem tegmentum from midline to lateral margin. This type of lesion (Fig. 9A) would include a medial region of the white matter that has been shown to be crucial for turning toward prey (Masino and Grobstein 1989). Two other animals had smaller lesions restricted to the lateral margin of the brainstem tegmentum which should have spared the medial region crucial for prey orientation (marked with X in Fig. 9B). Two additional animals served as surgical controls and had small lesions rostral to the VIIIth nerve.

All animals showed normal patterns of turning toward prey and away from looming stimuli prior to


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Fig. 6 "Main sequence" analysis of visually triggered orienting behaviors. Plots give relationship between peak velocity (top panel) or duration (bottom panel) and the total angular amplitude of a turn. Open symbols = escape turns [circles = hand presented card stimuli, triangles = computer generated looming stimuli]. Closed symbols = prey capture turns [circles = live mealworms as stimuli, tri- anoles = computer generated worm-like sitmuli]. Regression lines for escape turns are solid, those for prey capture are dotted

lesion. Both controls displayed turning following surgery which was similar to that documented here for normal animals. The frequency of response to stimuli and the directionality of their turning was statistically indistinguishable from their own prelesion behavior (P > 0.05, and see also Fig. 12).

In the case of the two animals with lesions extending across the tegmentum, both displayed marked changes in the directionality of prey capture and escape turning. As expected from previous reports (e.g. Kostyk and Grobstein 1987), these animals responded as frequently to prey stimuli presented in all areas of visual space as they had before lesion, but demonstrated a significant turning deficit for prey stimuli presented in the visual hemifield ipsilateral to the side of the lesion (Fig. 10, right side). In response to prey on that side, they consistently directed their responses inappropriately; straight ahead, or even slightly to the side opposite the actual

stimulus [percent correct (ipsiversive) turns decreased after lesion compared with prelesion, P < 0.001; total n = 215 trials]. Responses to prey stimuli in the visual hemifield contralateral to the lesion were not changed. Their deficit in escape turning was also unilateral and it had the same character as the deficit in prey capture: these frogs responded to looming stimuli presented from one visual field by moving straight ahead, or even turning inappropriately toward the stimulus. However, the misdirected turns were seen in response to stimuli presented in the visual hemifield contralateral to the side of the lesion, that is in the visual hemifield where prey capture was normally directed [Fig. 10, left side; percent correct (contraversive) turns decreased after lesion compared with prelesion, P < 0.001; total n = 283 trials]. Because this type of lesion affects escape and prey capture turning elicited from opposite sides of visual space, it indicates that descending tectal pathways for escape have an opposite laterality to those for prey capture (uncrossed vs. crossed, respectively). Nonethe- less the effects are consistent at the motor level. A left lesion alters turning responses toward prey stimluli in the left visual field (i.e. alters left turns) and alters turning responses away from looming stimuli in the right visual field (i.e. also altering left turns).

The two animals with more laterally placed tegmental lesions showed a dissociation of control for each type of turning: the direction of escape turns was altered, but prey capture turning was not altered. While both animals continued to turn correctly toward prey stimuli in both visual hemifields, they misdirected turns in response to looming stimuli presented in the contralateral visual hemifield (Fig. 11) [percent correct (contraversive) turns postlesion decreased from prelesion, P<0 .001 ; total n = 2 6 4 trials]. Postlesion responses to looming stimuli in the visual hemifield ipsilateral to the lesion remained statistically indistinguishable from prelesion. The laterality and character of these deficits in escape were the same as those induced by the larger lesions discussed above. The fact that prey capture turning was spared in these two animals is consistent with the hypothesis that there is a critical pathway for prey capture restricted to the medial part of the tegmentum (see brainstem sections, Fig. 9), and suggests that a critical pathway underlying escape maybe located more laterally in the tegmentum. The manner in which turning directions were altered in all animals (on both behavioral tests) is summarized graphically in Fig. 12. Clearly it is possible to alter the directionality of escape turning selectively, without necessarily altering turns made in response to prey-like stimuli.

Discussion

Catching prey and evading predators are both fundamental features of a frog's behavioral repertoire, and


Fig. 7A-C Schematic illustration of conventions for measuring and plotting the directionality of both types of turning behaviors. Scheme of measurement shown for escape (A) on the left, and for prey capture (B) on the right. As indicated in Methods, frame of reference for stimuli is opposite for the two behaviors, but extent of turn is measured the same way in each. (C) Cartesian graph displays the stimulus angle versus the measured angular amplitude of each turn. On such graphs, if stimulus angle were perfectly correlated with angle of turn, then data for escape turns would fall along the solid line, and data for prey capture turns would fall along the dashed line

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both begin with a turning component. These turning movements are quite similar on first inspection and, as discussed previously, the optic tectum controls both. Here we address issues that are fundamental to understanding the relationship between turning in these two behavioral contexts. (1) When Rana turns away from a looming stimulus does it represent the same motor pattern as that used when turning toward a small moving target? There is a closely related but not identi-

cal question: (2) ls turning in the two situations controlled by the same post-tectal circuitry?

Behavioral comparisons

Despite some superficial similarities between prey capture and escape turning (e.g., Figs. 3 and 4), the profile of velocities with which turns are executed is


m

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Fig. 9A, B Anatomical comparison of lesions with different behavioral effects.Brainstem sections from lesioned animals whose behavior is illustrated in Fig. 11 and 12. The level of the brain sections is indicated to the right. Both sections were taken from the area of the brainstem containing the largest amount of damage. A lesion invading both medial and lateral portions of the left brainstem (behavior in Fig. 10); B lesion restricted to the lateral area of the left brainstem (behavior in Fig. 11). CG = central gray, OT = optic tectum. The X in panel B indicates approximate location of the critical pathway for prey capture turning as defined by Masino and Grobstein (1989). Note that lesion in panel A damaged this area whereas lesion shown in B did not

consistently different for the two types of behaviors (Fig. 5). Main sequence analysis of duration and peak velocity (Fig. 6) also revealed that the control strategies for the two types of turns are noticeably different.

In some orienting behaviors, such as orienting head movements in rabbits (Collewijn 1977), there is sub- stantial variation in both turn duration and velocity as the angular amplitude of head movements changes. In other cases, such as turning movements of the head and saccadic eye movements in primates (Zangemeister et al. 1981; Bahill and Stark 1979) and head movements in owls (Knudsen et al. 1979), the strategy is to increase

peak velocity to achieve a greater turn angle, with duration maintained at a relatively constant level. In the frog orienting movements studied here, escape (by comparison to prey capture) appears to show a sac- cade-like "main sequence" diagram: while peak velocity of escape turns increased steeply with increasing angular amplitude, duration remained more constant. Note that in Fig. 6 there is essentially no overlap between escape turn data and prey orienting data. The kinematic differences evident from consideration of this figure argue strongly that the motor commands that underlie these two types of turning are functionally distinct.

It is important to note that the form of motor programs delivered by the animal could be influenced by the nature of the visual stimuli used to elicit them (e.g. Anderson and Brand 1993). However, our data showed that within each category of response (escape and prey capture) turns were not different when released with computer generated versus natural stimuli. For example, neither average duration of turn nor average peak velocity differed significantly (see results). Thus, the kinematic parameters reported here are valid de- scriptors of each behavior and did not depend upon stimulus parameters such as image velocity.

In comparing the spatial organization of the two types of turning, it is clear that the quantitative relationship between stimulus and response angle is more predictable for prey capture than escape. Our data for turns toward prey are consistent with other published data (e.g. Kostyk and Grobstein 1982, 1987) and show that turn angles closely match stimulus angles, so that a plot of the two variables yields essentially a straight line, y = x (Fig. 8, right side). In response to a visual threat, frogs typically turn away from a stimulus, but the particular angle of the turn is not perfectly matched to the angle of the stimulus. If one projected the line y = - x onto the plot of our escape turn data (Fig. 8, left side), most of the points would fall between that line and the X axis. This means that the frogs were usually turning away, but they did not turn far enough to be

Fig. 10 Example of a lesion Escape 180 deficit that included both types of turning behavior. Stimulus- response plots displaying �9 prelesion (black circles) and y oo 90 postlesion (open circles) ~xll~*~. ~ oo behavior from an animal with an b ~lk.~o .oO o extensive medial-lateral left . o ~ . o o brainstem lesion (see Fig. 9A). LI . o~ y_,,~, Data are plotted according to 1 80 "1 �9 conventions described in Fig. 7. Regression lines are for prelesion 9 0. data points and are provided to emphasize the trend in the prelesion data

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facing exactly away from the stimulus before they jumped. This is equivalent to the summary statement of Ingle (1991) that "the direction of escape elicited by a stimulus looming directly at the frog on a collision course is a compromise between leaping straight ahead to obtain maximum distance, and turning directly away from the threat."

While the greater angular variability of escape turning versus turns toward prey is clear, it must be remem- bered that the stimuli which are effective at eliciting escape are not spatially discrete (the card was quickly moved to subtend a considerable portion of one visual hemifield), whereas the typical insect stimulus for prey capture can be thought of as approximating a point target. In order to successfully evade predators, it is of utmost importance to respond quickly and move away from the impending attack. The exact angle of turn should not be as important as it obviously must be in

Fig. 12 Summary of lesion effects across animals in different lesion groups. Histograms summarizing percent "correct" turns for experimental and control animals. Correct turns were defined as turns away from the stimulus for escape and turns towards the stimulus for prey capture. In each histogram, open bars = responses to stimuli presented in left visual hemifield, stippled bars = responses to stimuli presented in right visual hemifield. Height = average % correct turns across animals; bars show range of percentages in individual animals. Left: pooled prelesion data from 6 animals. Right: postlesion data. Right top: data from two animals with lesions extending across lateral-medial (L&M) extent of brainstem. Right middle: data from two animals with lesions that were restricted to the lateral (L) brainstem. Right bottom: data from two controls. Asterisks indicate a stastically significant difference from the groups prelesion data (P < 0.001)

the case of catching a small prey item. Indeed, variability might be fundamentally important in the strategy of predator avoidance used by frogs, and may be an intrinsic property of the neural pathways controlling


escape (Grobstein 1992, 1994). In sum, it is clear from Figs. 6 and 8 that escape turning optimizes speed of execution, while prey orientation maximizes spatial accuracy. Finally, the differences in spatial organization and kinematics suggest a rather fundamental distinction between the motor" control circuitry for the orienting components of prey capture and predator evasion. This distinction should influence the extent to which theoretical models of the two behaviors rely on over- lapping functions (Corbas and Arbib 1992).

Post-tectal pathways

The marked differences between the characteristics of the two types of turning (see above) suggest that the underlying neural circuitry for prey capture and escape turning may be different. The retinotectal projection is responsible for determining the directionality of both types of turns (e.g. Ingle 1973, 1983; Ewert 1984). There- fore, at the tectal level, both behaviors are controlled by the same structure. However, the optic tectum gives rise to a number of efferent pathways, and it is at the post-tectal level that an anatomical separation of turning information could occur.

Lesions at the post-tectal level are known to produce changes in prey capture behavior that differ in both character and location from the changes in behavior that follow tectal lesions. We will compare alterations in escape with those in prey capture by considering first the location of deficits; their exact nature will be discussed below.

Unilateral damage to one tectal lobe produces a deficit in prey orienting responses in the contralateral monocular visual field, due to the largely crossed retinotectal projection (e.g. Kostyk and Grobstein 1982). Small unilateral lesions invading the ventromedial white tract of the medulla oblongata lead to a deficit in responding to prey stimuli located in the visual hemifield ipsilateral to the side of the lesion (Masino and Grobstein 1989). Since the laterality of this deficit is opposite to that of unilateral tectal lesions, a crossed tectofugal pathway has been implicated in the trans- mission of information from the tectum to downstream centers involved in prey capture (There may also be a small uncrossed component, but it has been less well characterized and will not be considered at this point.) We found that unilateral lesions of the brainstem (such as those illustrated in Figs. 10 and 11), produced a deficit in turning in response to looming stimuli in the contralateral visual hemifield. Thus escape turning appears to be dependent primarily upon an uncrossed tectofugal system.

That there is a real distinction between the post- tectal escape and prey capture pathways can be seen within the behavior of a given animal since the deficits for each behavior show up on opposite sides of the visual world (Fig. 10). It should be noted that these

lesions are not necessarily disrupting the descending axons of tectal cells themselves, but could be disrupting axons of interneurons that are one or more synapses "downstream" from tectal cells. There is already evidence that the post-tectal prey capture pathway involves a tegmental relay (Masino and Grobstein 1989), and there is some evidence that our lesions may have im- pinged on fibers derived from a tegmental relay (Roche and Comer 1994 and unpublished).

The descending pathways for each type of turning are also clearly distinguishable on the basis of discrete lesions. Small, laterally placed lesions only altered escape turning while prey capture turning remained basi- cally unchanged. It will be important now to follow up this observation and determine if small medially placed lesions will produce deficits in prey capture turning (as described by Masino and Grobstein 1989), without concomittant deficits in escape. A double dissociation has already been shown in rodents in which selective lesions in collicular output pathways abolish one type of response while sparing the other (Ellard and Good- ale 1986, 1988; Dean et al. 1986). This suggests that anatomical separation of the tectofugal pathways controlling turning toward and turning away may be a general organizational principle for the vertebrate midbrain.

Despite the distinctions outlined above, there is a consistency in the effects of tegmental lesions that should be emphasized. If the consequences of unilateral lesions are described in a motor frame of reference, then in the case of each behavior, lesions on one side of the nervous system only affect turning in one direction, and it is the same direction for each. For example, tegmental lesions on the left side alter the ability to initiate appropriate escape turns to the left, and they alter the production of prey capture turns to the left. Thus, access to the motor circuitry for turning is fully lateralized at this level of the CNS. This would seem to be consistent with current models for the tectal control of orienting functions (e.g. Corbas and Arbib 1992).

Finally, we would call attention to the character of the deficits that follow unilateral lesions of the post- tectal circuitry. While tectal lesions produce a scotoma in the region of the visual field that would be mapped to the removed tissue, lesions of the post-tectal circuitry do not lead to a scotoma in the usual sense, but rather to a distinctive syndrome wherein responses for part of the visual field are systematically misdirected. Such misdirected movements have been documented before for orienting responses to prey (Kostyk and Grobstein 1982, 1987) and are completely consistent with our data on tegmental lesions and prey capture. Furthermore, we have shown that this syndrome of shifts in turning directions holds for escape turning as well (see Figs. 10, 11 and 12).

This type of directional deficit has not been reported often for unilateral lesions, although some other examples can be found. These include the sound-


evoked saccadic head movements of owls (Wagner 1993), amphibian water wave orientation (G6rner et al. 1984), and insect wind and touch evoked escape turning (see Comer and Dowd 1993). It is therefore worth entertaining the idea that visually triggered escape turning and prey capture share not only some basic features in integrative processing with each other, but that there may be a type of circuitry used for orienting behaviors that is useful to organisms as diverse as insects, amphibians and birds.

Acknowledgements This research was supported in part by funds from the Department of Biological Sciences, University of Illinois at Chicago. We thank F. Yeung and Jennifer Sandman for assistance with some of the procedures, and Paul Grobstein, A. Don Murphy and J. Patrick Dowd for comments on an earlier version of this manuscript.

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