Perception of Visual Motion Coherence by Rats and Mice

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Vision Research 46 (2006) 2842–2847 www.elsevier.com/locate/visres

Perception of visual motion coherence by rats and mice

R.M. Douglas a,b,¤, A. Neve b, J.P. Quittenbaum b, N.M. Alam a, G.T. Prusky b

a Department of Ophthalmology and Visual Sciences, University of British Columbia, 2550 Willow Street, Vancouver, BC, Canada V5Z 3N9 b Canadian Centre for Behavioural Neuroscience, The University of Lethbridge, 4401 University Drive, Lethbridge, Alta., Canada T1K 3M4

Received 13 November 2004; received in revised form 17 January 2006

Abstract

The coherence thresholds to discriminate the direction of motion in random-dot kinematograms were measured in rats and mice. Per- formance was best in the rats when dot displacement from frame-to-frame was about 2 degrees, and frame duration was less than 100 ms. Mice had coherence thresholds similar to those of rats when tested at the same step size and frame duration. Although the lowest thresholds in the rats and mice occasionally reached human levels, average rodent values (»25%) were 2–3 times higher than those of humans. These data indicate that the rodent and primate visual systems are similar in that both have local motion detectors and a system for extracting global motion from a noisy signal. © 2006 Elsevier Ltd. All rights reserved.

Keywords: Extrastriate cortex; MT; Random dot; Kinematograms; Visual water task; Psychophysics

1. Introduction is, however, an open question whether primates have unique cortical capabilities, or whether such a functional The detection and eVective use of visual motion is organization is a fundamental property of mammalian widespread in the animal kingdom. Experimental investi- visual systems. If extrastriate analysis of global visual gations of the neural mechanisms of motion perception motion is common to mammals, this would have implica- have been conducted in species as diverse as Xies, pigeons, tions for its evolution and ecological utility. In addition, and monkeys (CliVord & Ibbotson, 2002), and simple studying motion perception in laboratory rodents would neural circuits capable of detecting local motion of single facilitate experiments into the cellular and molecular elements have been studied in the Xy (Reichardt, 1961) substrates of visual motion processing. To this point, and rabbit retinas (Barlow & Levick, 1965; Fried, Munch, however, no systematic study of motion perception has & Werblin, 2002). In recent years, it has become common been conducted in rodents, largely because it has been too to use dynamically moving random-dot patterns (or diYcult to test their visual motion thresholds psycho- kinematograms) to assess visual motion, as they enable physically. Over the past several years, we have used the the study of motion perception in the absence of posi- Visual Water Task (Prusky, West, & Douglas, 2000) to tional or form cues (Nakayama & Tyler, 1981). Percep- quantify acuity and contrast sensitivity thresholds in rats tual mechanisms that can detect common motion of and mice (McGill, Douglas, Lund, & Prusky, 2004; Pru- many elements have been identiWed in humans and other sky et al., 2000; Prusky & Douglas, 2004), and we report primates (Braddick, 1974; Morgan & Ward, 1980; Wil- here that this task can be adapted to measure their visual liams & Sekuler, 1984) and localized to extrastriate cor- motion thresholds. tex (Baker, Hess, & Zihl, 1991; Newsome & Paré, 1988). It In order to determine whether rodents have visual motion capabilities and anatomical substrates comparable * Corresponding author. Fax: +1 604 876 6553. to primates, we compared the dot motion coherence thresh- E-mail address: [email protected] (R.M. Douglas). olds of rats with those of humans.

2. Methods 2.3. Stimuli

2.1. Subjects Kinematograms were computed separately for each monitor before every trial, and were then played continuously until the end of the trial. A Six adult female Long–Evans rats and six adult C57BL/6 mice were random-dot kinematogram consisted of 24 frames or images. The diame- used in the experiments. The animals were between 90 and 150 days of age ter of the round dots was 1.9° for the rats, and 2.9° for the mice as studies at the start of training, and testing continued over the subsequent 4–6 from our laboratory (e.g., Prusky et al., 2000) have shown that the grating months. All procedures were authorized by the University of Lethbridge acuities of Long–Evans rats and C57BL/6 mice are 1.0 and 0.55 cycles per Animal Care Committee, which approves procedures that are conducted degree (c/d), respectively. The total area of the dots was about 20% of the in accordance with the standards of the Canadian Council on Animal screen area, and this corresponded to there being 62 (rats) or 28 (mice) 2 Care. dots on each image frame. The dots had a luminance of 96 cd/m and the 2 To facilitate comparison with human motion vision, three human background was 1.1 cd/m . observers viewed the same stimuli from the same distance. They used Each dot could move from one frame to the next, or disappear. The pushbuttons to start each trial and to record their decisions about which step size, or amplitude of the displacements from fame to frame, was the side had the positive stimulus. Human testing was conducted in accor- same for all dots, with only the direction of movement varied between dance with the guidelines of the University of Lethbridge Human Subjects frames. Motion noise was introduced by having a percentage of the dots Research Committee. move in random directions (Fig. 2) with the additional constraint that there was no net movement. The remainder of the dots all moved in one, 2.2. Apparatus coherent direction. Dot displacements of 0.24°, 0.47°, 0.94°, 1.88°, 3.77°, 5.65°, and 7.54° were used in diVerent blocks of trials. The Visual Water Task (Prusky et al., 2000) uses a trapezoidal tank After moving for 2 or 12 frames (lifetime) each dot was randomly repo- (120 cm L £ 80 cm W £ 26 cm W £ 55 cm H) with two ViewSonic EF70, sitioned, thus ensuring a constant number of dots on screen. A constant 17Љ computer monitors facing into one end (Fig. 1). A midline divider percent of dots died and were reborn elsewhere on each frame, and motion (46 cm) extends into the pool from between the monitors, each of which wrapped from the 24th to the 1st frame so that the kinematogram could be subtended about 30° degrees when viewed from the end of the divider. The played continuously. Longer lifetimes were not possible with a looping tank was Wlled with water, and an escape platform was placed just below requirement, and thus dot lifetimes of 2 and 12 frames limited the maxi- V the surface directly under one of the monitors. The platform was always mum e ective coherence to 50 and 92%, respectively (Bischof, Reid, Wylie, located below the positive (+; reinforced) stimulus. Visual stimuli were & Spetch, 1999). generated by, and the experiments were controlled with custom software. Frame duration set the stimulus onset asynchrony (SOA) for the dots to appear on two successive frames, and frame duration was a multiple of the video screen refresh rate. In the experiments with rats, 1, 2, 4, 8, 13, 19, and 26 screen refreshes were employed. As the monitors had an 85 Hz vertical refresh rate, these values translate to frame durations of 12, 24, 48, 94, 153, 224, and 306 ms. Video – + Monitors 2.4. Behavioral testing The animals were trained to associate swimming to the positive stimu- Submerged lus, regardless of its left/right location, with escape from water. The initial Platform training consisted of training the rat or mouse to distinguish between 100 and 0% coherence. Rats learned to grasp the end of the divider and inspect both screens before making a choice; mice tended to slow down at the bar- rier and swim back and forth before making a choice. After an animal had Wnished a trial, it was returned to a holding box to dry and groom while the other 5 animals completed the same trial. Sessions consisted of 15–20 Choice trials per animal. The training kinematograms had a step size of 0.471°, a Plane frame duration of 12 ms, and a lifetime of 10 frames. Once the rats reached at least 80% accuracy over a block of 10 trials, we changed the task to identifying the direction of motion. This had the advantage that the kinematograms on the two monitors were identical in coherence, step size, frame duration, and lifetime, and only diVered in

Water 0% Coherence 100% Coherence

Start Point

Fig. 1. Schematic top-view of the Visual Water Task. The task uses a trapezoidal pool with two computer monitors at one end displaying either a pos- Fig. 2. Schematic diagram of stimulus attributes. Motion coherence dis- itive (+, reinforced) or negative (¡, non-reinforced) stimulus. An escape plays consisted of multiple dots that could move in any direction across platform is placed below the monitor showing the positive stimulus and the frames. After moving on 2 or 12 successive frames, the dot disappeared left/right position of the pair is randomized. The platform surface is just and a new dot was created at another random location on the screen below the water level and is not visible to the animal. Animals are released (dashed circles). At 0% coherence, all dots moved in random directions at one end and they swim to the end of a divider where they inspect the two with the average being zero. At maximal coherence all moving dots moved monitors before choosing one arm of the maze to swim into. coherently in one direction. 2844 R.M. Douglas et al. / Vision Research 46 (2006) 2842–2847 direction of the coherent motion. For the rats, the discrimination was grams, and did so even when coherence was 25% or less. between leftward (negative) and rightward (positive) coherent motion. For The directional discrimination, however, was a diYcult test the mice, the task required a discrimination between horizontal (positive) for the animals to learn. Initially we tried testing the rats and vertical (negative) motion. Coherence thresholds were then established by reducing the percent of with a dot lifetime of 2 frames, but none of the rats could dots moving coherently for blocks of ten trials. A preliminary threshold learn to make the discrimination. This may have been was established when performance fell below seven correct in a block of 10 because 50% was the maximum coherence possible with trials. The threshold was assessed several times or until a reliable pattern single frame motion. When dot lifetime was increased to 12 of performance was generated. Generally, three or four estimates were so frames we could start testing at 92%, and the animals had obtained. fewer problems learning, taking 86 trials on average to 3. Results learn the new discrimination (range 30–200 trials). Once the rats learned the task, performance was close to perfect at 3.1. Behavior and training high coherencies, and then declined as the percentage was decreased (Fig. 3). Testing was discontinued once perfor- All the rats and mice were eventually able to discrimi- mance dropped below 70% because animals rapidly become nate the direction of motion in random-dot kinemato- confused when they made many errors. Although most of the experiments used dot lifetimes of 12 frames, we tried reducing dot lifetime later, after the rats had had extensive 100 experience with task. On the second attempt, all of the rats 90 were able to discriminate the direction of motion with two- frame lifetimes, but there was no signiWcant diVerence in 80 coherence thresholds for 2-frame (31.0 § 2.85) and 12-frame motion (25.21 § 4.59) kinematograms (t D 1.0, df D 5, 70 p D 0.36). We attempted to train the mice in the same way as the 60 rats, but they could not learn the initial discrimination of

% Correct maximal coherent motion versus one that had no coherence 50 (i.e., 0%). After this initial failure, we tried training the mice on an alternative task in which the requirement to discrimi- 40 nate between horizontal motion (+) and vertical motion (¡). This they did learn in an average of 360 trials (range 0 102030405060708090100 262–520). Like the rats, once the mice had learned the task, % Coherence they could perform at a high level. Fig. 4A shows one mouse making only occasional errors over 544 trials as Fig. 3. Performance of the rats for kinematograms with a dot displace- coherence was lowered progressively six times. Perfor- ments of 3.8° per 47 ms frame. Testing started at 92% coherence, and that mance improved over the experiment: Initially the mouse was reduced until performance dropped below 70%. This was repeated several times, and an average of 239 trials was needed to establish the started making errors at dot coherencies of 60%, but on threshold for each animal. Each point is the mean percent correct for the 6 subsequent runs the mouse made fewer errors and the animals, and the error bars are for one standard error. threshold stabilized at about 25%. On average 449 (§4.1)

AB100 100 100 90 90 90 80 % Coherence ( ) 80 70 80 60 70 70 50

% Correct 60 % Correct 60 40

50 30 50 20 40 40 10 0 0 100 200 300 400 500 0 102030405060708090100 Trial % Coherence

Fig. 4. (A) Example of coherence threshold testing in one mouse. Initially the mouse made errors almost as soon as the coherence was reduced, but with further testing, performance stayed near 100% until the coherence had dropped to below 30%. (B) The average performance of the 6 mice are plotted as a function of coherence. The error bars show one standard error above and below the means. R.M. Douglas et al. / Vision Research 46 (2006) 2842–2847 2845

A 100 trials were used to measure one coherence threshold. The 90 corresponding threshold in rats was obtained more rapidly (239 § 9.9 trials) but with a shallower frequency-of-seeing 80 curve (Fig. 3) than that for the mice (Fig. 4B). 70 Rats 60 3.2. Dot motion 50 40 In the Wrst quantitative experiment with the rats, dot 30 step size was varied and coherence thresholds were lowest 20 between 1° and 4° (Fig. 5A). At 26.9%, the rat thresholds

Coherence Threshold (%) were 3.9 times that of the average of 6.8% for the humans 10 Humans over the same range. The coherence thresholds were higher 0 0.2 0.4 0.6 1.0 2.0 4.0 6.0 8.0 for both rats and humans at larger step sizes, and at 7.54° Displacement per Frame (degrees) two rats were unable to discriminate at the maximum available coherence of 92.5%. Smaller step sizes were also chal- B 100 lenging for the rats, whereas humans had little trouble with the same sizes, or even at 0.047° at which their threshold 90 was 10.4% (not shown). 80 The average rat thresholds were higher than the human 70 Rats thresholds for all frame durations (Fig. 5B). The lowest, 60 22.9%, was 2.2 times higher than the corresponding 24 ms 50 threshold for the three humans. Rat thresholds became pro- 40 gressively higher for longer durations, whereas the human thresholds varied little. Four of the six rats were unable to 30 discriminate when the frame duration was 306 ms. 20 Humans

Coherence Threshold (%) Changing either the size of the jumps a dot makes, or the 10 time between the jumps can vary the speed of dot motion. 0 The data from Figs. 5A and B are replotted in Fig. 5C as a 10 20 40 60 100 200 400 function of velocity. The two speeds from the two experi- Frame Duration (ms) ments cover the same velocity range, and the coherence ¡1 ¡1 C 100 thresholds are similar and low for the 20° s to 80° s range, but diverge at each extreme. At higher velocities, a 90 lower threshold was present when the increase in speed was 80 Varying Frame due to shorter frame durations than it was with larger step 70 Duration sizes. Conversely at low velocities, small step sizes were 60 more discernible than long frame durations. 50 40 4. Discussion 30 Varying All the rats and mice learned to discriminate the direc- 20 Displacement tion of random dot kinematograms. The lowest coherence Coherence Threshold (%) Coherence Size 10 thresholds were about 20–25%, which was higher than 0 4 6 8 10 20 40 60 100 200 400 that of humans, but comparable to those in cats (Rudolph & Pasternak, 1996). The experience in our laboratory is Velocity (degrees/second) that mice are harder to train and test, and do not perform Fig. 5. EVects of varying dot step size and delay on coherence thresholds. as well as rats in visual tasks. They have a lower acuity (A) Rat and human motion coherence thresholds for displays with dots and contrast sensitivities, and we expected that they V W moving di erent distances per frame. Each lled circle indicates the aver- would not do as well with motion coherence. The fact they age value for the six rats, and open squares depict the average for 3 human observers. Two rats were unable to discriminate above 70% accuracy at did as well as the rats may have been due to the use of an the largest step size. Frame duration was 48 ms. (B) Motion coherence “easier” task. Discriminating vertical from horizontal thresholds for displays with diVerent frame durations (and thus diVerent motion may be an easier task than leftward versus right- stimulus onset asynchronies). Four rats were unable to discriminate at ward motion. This could be a cognitive problem with the better than 70% accuracy for the largest SOA. Dot displacement was directional signal having a much lower saliency than the 3.78°. (C) Changing either dot displacement or frame duration alters the speed of the dots. The data from (A and B) are plotted here as a function orientation signal. Alternatively, the local motion detec- of velocity. The two manipulations were not equivalent as diVerent thresh- tors may be oriented, but not directional selective, and olds were obtained for the same speed. The error bars show one standard this would make the leftward versus rightward discrimina- error around each mean. tion impossible. 2846 R.M. Douglas et al. / Vision Research 46 (2006) 2842–2847

4.1. Global motion ment (Dmax) of about 8° (Fig. 5A). This is a much larger W Dmax than the 0.25° rst found by Braddick (1974), and is The present results clearly demonstrate that rodents most likely due to the much large dot sizes (Morgan, 1992), have a global motion system. The tasks can not be solved long lifetimes (Todd & Norman, 1995), and large display by tracking a single dot. Rather, information about many areas (Eagle & Rogers, 1996) which extended into periph- dots must be integrated over a larger part of the visual Weld. ery (Baker & Braddick, 1985). Another way to look at the In primates, the biological basis of the perception of motion data is to consider that, for the rats, the large dots are coherence has been thought to rely on the area around MT, roughly equivalent to the small dots used in many human as lesions there impair the extraction of a motion signal studies. If one scales a typical human Dmax of 0.25° by the V from a noisy display (Baker et al., 1991; Newsome & Paré, 30-fold di erence in acuity, one gets an predicted Dmax of 1988). Similarly, area PMLS in the cat appears to be spe- 7.5° for rats. These considerations suggest that the rats and cialized for motion processing, and lesions of PMLS impair humans have local motion systems that have very similar motion coherence perception (Huxlin & Pasternak, 2004; properties when working at the same spatial scale. Rudolph & Pasternak, 1996). At present, there is no electro- Frame duration or stimulus onset asynchrony (SOA) is physiological evidence for a homologous extrastriate area also critical for obtaining apparent motion, and the rats in rat, but induction of c-fos immunoreactivity in the area had increasing diYculty as SOA increased and were quite after viewing moving stimuli has suggested that rat antero- poor beyond 150 ms. Similar limits have been seen in lateral (AL) visual area is the equivalent of primate MT human studies of random-dot motion using small dots and cat PMLS (Montero & Jian, 1995). (Braddick, 1974), but the human performance reported In the present study, human thresholds were consistently here is quite diVerent as it was good across all SOAs tested. lower than the rat thresholds for the same stimuli, usually This may be because the optimal (and presumably maxi- by a factor of 2–4, and sometimes by much more. This dis- mal) delay grows with larger dot displacements (Eagle & crepancy is probably a diVerence in their visual capabilities Rogers, 1997). and not due to the animals giving up when the task became Y more di cult. Performance was often close to 100% until 5. Conclusions the coherence approached the eventual thresholds, and the W nal threshold estimates were consistent across animals. The limited spatial and temporal ranges for dot move- Interestingly, Bischof et al. (1999) report that pigeons also ment are consistent with simple local motion detectors have motion coherence thresholds much higher than being used in the rodent to detect individual dot motion. W humans. Coherence thresholds of 10–20% in guppy sh The low thresholds for motion coherence are evidence for a have been reported (Anstis, Hutahajan, & Cavanagh, 1998) more global mechanism that combines the output of these so it may be that all vertebrate visual systems have some detectors. Although the visual capabilities of rodent are ability to extract motion in the presence of noise. This func- more limited than in primates, there are advantages of tion may be partly localized in rat to AL and in cat to LS, using rats and mice as a experimental models in uncovering but the homology to primate MT is not exact, as these areas the fundamental mechanisms underlying the perception of W do not appear to be as pro cient as MT is in the primate. visual motion. 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