COLOR PERCEPTION AND OBJECT RECOGNITION IN A LAKE MALAWIAN CICHLID MELANOCHROMIS AURATUS
Jeremy Didion
A Thesis
Submitted to the Graduate College of Bowling Green State University in partial fulfillment of the requirements for the degree of
MASTER OF SCIENCE
December 2012
Committee:
Robert Huber, Advisor
Moira J. van Staaden
Jeffrey G. Miner
© 2012
Jeremy Didion
All Rights Reserved
iii ABSTRACT
Dr. Robert Huber, Advisor
Cichlids of the African Great Lakes offer a remarkable model system for studying the functional components and perceptual constraints of visual perception, as it is the primary modality in sensory-driven speciation. An objects distinct features may be used in visual recognition. Here we show that color is more salient than shape in the object recognition of the
Malawian cichlid Melanochromis auratus. Using a food-reward operant conditioning paradigm, fish were trained to discriminate between ecologically neutral objects (i.e. red triangle, blue square). Probe trials confirmed that M. auratus discriminated between the rewarded stimulus and the distractor, while the dissociation of these objects allowed for the assessment of the relative salience of color and shape information. Results indicate a clear precedence of color over shape information (Sign Test 13/16 p = .021). Moreover, we have demonstrated that the best absolute and difference visual thresholds for hues (color) in M. auratus are biased towards blue colors.
Using an unconditioned optomotor response towards moving vertically grated bars, absolute visual thresholds were lowest in the range of primary absorption of M. auratus‘s single cones
(414 nm).
iv I would like to dedicate this thesis to my father Dennis Didion who is sorely missed.
Without his guidance and his lessons in perseverance this project would not have been possible.
v ACKNOWLEDGEMENTS
I am forever grateful to my advisor Robert Huber for his patience, advice, technical support, statistical analyses, writing and review of the various stages of this project. I am also appreciative for the comments and suggestions provided by my committee members Moira van
Staaden and Jeffrey Miner. I am also thankful for the continuous support and wonderful suggestions from the present and past members of the Huber and van Staaden labs.
This study was made possible with the support of my mom, Susie Didion, my sister,
Jenny Didion, and my life-long friends Garren Schaffer and Josh Smith. Also, a special thanks to
Elise, for her love, patience, and support throughout this entire stage of my life.
Support for this research was provided by the J. P. Scott Center for Neuroscience, Mind,
& Behavior, BGSU, and the Department of Biological Sciences, BGSU.
vi
TABLE OF CONTENTS
Page
CHAPTER I. OBJECT RECOGNITION IN A LAKE MALAIAN CICHLID,
MELANOCHROMIS AURATUS ...... 1
Introduction...... …...... 1
Materials and Methods ...... 3
Result……...... 7
Discussion...... 12
References...... 16
CHAPTER II. COLOR PERCEPTION IN A LAKE MALAWIAN CICHLID,
MELANCHROMIS AURATUS ...... 20
Introduction...... 20
Materials and Methods...... 22
Results...... 27
Discussion...... …...... …...……...…...…...... 32
References...... 36
APPENDIX I: IACUC APPROVAL ...... 40 vii
LIST OF FIGURES
Figure Page
1 Experimental tank for operant conditioning and dissociation trials ...... 5
2 Sample learning curve for one of eight fish during shaping of the operant
behavior...... 8
3 Acquisition of the operant behavior as indicated by association time in probe
trials...... …...... 10
4 Relative use of color and shape information as indicated by association time in cue-
dissociation tests ...... 11
5 Experimental tank for characterizing color perception ...... 23
6 Radiometric characterization of a range of display colors presented on a Dell 1908FPb
monitor...... 25
7 Minimum brightness required for perception of different colors in four different
individuals of Melanochromis auratus ...... 28
8 Minimum brightness perception for different hues of the color spectrum in M.
auratus...... 30
9 Color discrimination in M. auratus………………………………………………… 32
1
CHAPTER I: OBJECT RECOGNITION IN A LAKE MALAWIAN CICHLID,
MELANOCHROMIS AURATUS
INTRODUCTION:
The visual system accomplishes recognition by breaking down complex visual stimuli into individual features (Logothetis & Sheinberg, 1996). The relative salience of object features, has been shaped over evolutionary time to facilitate a focus on regions of greatest interest and relevance. Reducing the whole image into its features decreases computational complexity, time to detection, and the discrimination of biologically important stimuli. By targeting particularly salient features, such as shape, color, motion, size, or luminance, an organism could make substantial gains in both information content and processing efficiency.
Color and shape are fundamental aspects of visual perception. Color perception is dictated by the spectral sensitivities of photoreceptors and their interaction with the central processing in the brain. Behavioral experiments of performance on visual tasks can reveal the interactions between these photoreceptors and how the information is processed in the brain.
Behavioral conditioning is a powerful tool, which not only indicates the capacity of the receptors, but also directly represents the sensory information available to the animals for controlling their actions. The sensory mechanisms underlying this ability for processing and storing information on compound visual stimuli, have been explored using operant conditioning in a variety of taxa, including honeybees (Gould, 1984), pigeons (Reynolds, 1961; Johnson &
Cumming, 1968), macaques (Cantlon & Brannon 2005), goldfish (Ohnishi, 1991), and cichlids
(Allen & Fernald 1985; van Der Meer & Bowmaker, 1995).
Visual discrimination studies in teleosts have revealed features of the sensory systems, as 2 well as more cognitive aspects of visual processing such as global and local dimensions of hierarchical stimuli (Truppa et al 2010), the perception of illusory contours as real borders
(Wyzisk & Neumeyer 2007), and feature extraction mechanisms underlying complex object recognition tasks (von der Emde & Fetz, 2007). Shape discrimination has been extensively explored in the goldfish (Carassius auratus) and several other taxa, demonstrating successful discrimination between simple two-dimensional visual stimuli (common geometrical shapes) but also more complex images and 3D objects (Schluessel et al, 2012; Sovrano & Bisazza 2008).
Color discrimination studies have shown that damselfish (Pomacentrus amboinensis) can quickly associate a colored stimulus with a food reward (Siebeck et. al., 2008).
Cichlids of the African Great Lakes constitute the largest and most remarkable of vertebrate radiations (Kornfield & Smith 2000; Kocher 2004; Seehausen 2006). Renowned for their rich diversity, they offer a unique opportunity to study adaptive changes in rapidly evolving species flocks. These fish possess an impressive array of color patterns (Carlton, 2009) with many studies implicating visual communication as the basis for mate choice (Seehausen & van
Alphen, 1998; Couldridge & Alexander, 2002; Smith & Kornfield, 2002), leading to variation in visual capabilities, which may have influenced the speciation of cichlids. Interpretations of complex multicomponent signals may also underlie the recognition of predators and prey
(Dobberfuhl et al., 2005), and encode spatial information for navigation (Braithwaite & Burt de
Perera, 2006). Much is known about the molecular underpinnings of cichlid vision (Carleton,
2009; Hofmann et. al., 2009; Smith et. al., 2011). However, we know surprisingly little about how other aspects of the visual system are tuned for survival (e.g. what is the relative salience of luminance and movement information, how do perceivers parse their visual world into organized units). By integrating the psychophysical and behavioral bases of visual communication in 3 cichlids we can provide input for the larger question - by what mechanism did this diversity evolve?
Melanochromis auratus is a mouth-brooding African cichlid, widely distributed in the southern portion of Lake Malawi, where it commonly occupies relatively shallow (1.5-10 m), rocky habitats rich in algae (Ribbink et al 1983). It features striking, sexually dimorphic coloration; juveniles and females are bright yellow with horizontal black and white stripes on the upper half of the body, whereas adult males are black with light blue or yellow stripes. The visual system appears to have little variation in opsin gene expression, and the species is relatively unaffected by variation in rearing light conditions (Hofmann et al, 2010). As a first step in determining how the visual system is tuned for survival in a generalized Malawian cichlid here we: (1) condition M. auratus to ecologically neutral artificial objects in a two-choice, food- reward operant conditioning paradigm, (2) assess the acquisition of the operant behavior by using association time as a measure of individual preference in probe trials, and (3) we test the relative salience of color and shape information in object recognition by reallocating these visual properties in dissociation tests.
MATERIALS & METHODS
Subjects:
Eleven captive-bred individuals of Melanochromis auratus (6 F, 5 M; Length 80-110 mm) were obtained from a commercial supplier (PetSolutions, Ohio, USA). Fish were maintained individually in subdivided 20-gallon aquaria (i.e. 3 fish per tank) at 24-26° C, 7.8-8.5 pH, and a light cycle of 12L:12D.in the Animal Facility at Bowling Green State University. A layer of gravel and Terra Cotta pots provided digging opportunities and shelter. Animals were fed Vegi Flakes (Ocen Nutrition, Utah, USA) daily except during conditioning when they were 4 fed only in the experimental tank with mini-pellets (Hikari, Kansai, Japan). Three animals were excluded from the experiment after two months, as they were uncooperative or failed to reach criterion. All experiments were conducted in accordance with the guidelines established by
Bowling Green State University’s Institutional Animal Care and Use Committee (IACUC) under protocol #11-002 (Appendix 1).
Apparatus:
All conditioning and behavioral trails were conducted in a darkened room, with only light emitted from the LCD screen. The apparatus (Fig.1) consisted of an opaque-walled experimental arena (Fig.1) with an LCD screen (Digital 8.5" CARTV) fitted into a (65x155 mm) window of on one side. An opaque vertical partition (5 x 100 mm long) bisected the entire LCD screen vertically, forcing the fish to move either to the left or right side of the screen. Filtration and aeration were removed during behavioral trials. Food rewards were presented via two feeding tubes that extended through the opaque lid of the experimental arena in front of the left and right screen image. Fish movements were recorded with a centrally placed, overhead video camera
(SVAT CCDBW mini digital spy) linked to an Apple Macintosh running custom tracking software based on routines provided through the freeware JavaGrinders library (available for1 download at
O
L R
LCD screen
Fig. 1. Experimental tank for operant conditioning and dissociation trials (295 x 295 x 230 mm water depth). The tank was separated into three sections: two choice areas (145 x 100 mm) on the left [L] and right side of the partition [R], and the remaining area of the tank [O]. A camera [X] was placed in the center, overhead. Grey circles represent the feeding tubes extending into the tank on either side of the partition.
Procedure:
Operant conditioning:
Fish were conditioned with food reward to one of two shapes of identical aspect ratios
(1:1): a blue square or a red triangle. Colors were selected to be of equal brightness according to the known visual spectrum of M. auratus (Jordan et al 2006, and chapter 2 of thesis). During training and testing two images were projected onto the attached LCD screen. Each training session commenced with a 10-minute acclimation period during which a white screen was presented. This was followed by a 15-minute period in which the two test stimuli were presented on both sides of the screen. The side of the rewarded stimulus was chosen at random and it remained on screen until the fish associated with it. The behavioral response was shaped by initially rewarding any approach to the conditioned image, and in subsequent training sessions, progressively increasing the wait time to reward from 3 seconds up to a maximum of 30 seconds.
The image then reverted to a white image until the fish left the rewarded area, followed by a new 6 presentation of the two images on randomized sides. The number of presentations per 15–minute training session varied from 6 to 24 depending on the activity level and motivation of the test subject. All fish received 20±3 training sessions with variable maximums (15-30 sec) reached around the 18±2 session. Training sessions occurred at 1-2 day intervals.
Probe trials:
To assess how well each fish had learned their respective image, two probe trials were conducted without food reward. In each of these, a 10-minute acclimation period with a white screen was followed by a 5-minute testing period in which the conditioned and the unconditioned stimulus were presented continuously on the screen. A second trial, separated by a single
(rewarded) training session and a rest day, duplicated the experiment with reversed image positions. The fish's position was tracked during all probe trials in order to obtain a measure of association time with each section of the experimental arena. Following the two probe trials, all individuals received two further conditioning sessions with rewards to reinforce learning.
Dissociation tests:
Following the probe trials and two conditioning sessions, fish were subjected to a set of two dissociation tests without food reward. To assess the relative salience of color and shape information, color and shape information of the test stimuli were reversed, the red square and blue triangle were replaced with a blue triangle and red square. A 10-minute acclimation period with a white screen was followed by a 5-minute testing period in which the reversed images were presented on a randomized side of the screen. In the second trial the images were presented on the opposite side. The two dissociation trials were separated by a single training session (non- dissociated and rewarded) and a rest day.
Data analysis: 7 In all choice tests (probe and dissociation), each individual was tested twice with the stimulus pairs balanced for presentation on both left and right sides of the screen. The trials are not independent of each other, so each individual’s probe and dissociation tests were grouped together and subsequent t-tests were performed. For data from probe trials a one-tailed t-test compared each fish’s preference against an external hypothesis mean of 0.5 to test whether significantly more time was spent in front of the conditioned image compared to the unconditioned one. The p-value was adjusted for multiple comparisons using Dunn Sidak (Sokal
& Rohlf, 1995). Two-tailed t-tests were used for dissociation trials to determine if a significant difference existed in the amount of time spent in front of the reinforced color or shape. Sign
Tests were employed to discern whether the experimental animals made consistent trends in choices across trials in both the probe and dissociation tests.
RESULTS
Acquisition:
Initially, individuals were required to remain stationary in front of the reinforced image for at least 5 seconds in order to receive a reward. The length of time before reward administration was slowly increased so fish would spend more time next to their conditioned image. The interim criterion for behavioral shaping, seven rewards within a 15-minute training session, was attained by eight individuals within 8-12 training sessions. One individual exhibiting an extreme side bias, and two individuals who were unwilling to approach the LCD screen, were excluded from further training. The operant behavior was shaped with 1 second of additional wait time to reward per conditioning trial, generating a roughly linear learning curve
(data not shown). A typical conditioning profile for the type of learning curve obtained in the object discrimination task is shown in Fig. 2. During training, blue square and red triangle used 8 as rewarded stimulus did not differ in the number of trials needed to reach the learning criterion between.
25
20
15
10
verage time till reward (sec) 5 A
0 0 5 10 15 20 Training Session Fig. 2. Sample learning curve for the shaping of the operant behavior in a single fish. The line represents the average amount of time waited in front of conditioned image, before reward administration, which increased as the number of training sessions. In this particular fish a maximum of 25 seconds was reached around the session 19.
Probe trials:
The overall association time with the rewarded stimulus for each fish in the probe trials
(Fig. 3) averaged 192.1 seconds (trial 1) and 253.7 seconds (trial 2). This amount of time exceeds the expected 150 seconds if fish were to spend either side of the LCD screen at random.
Regardless of the side of the screen on which the image was presented, fish spent significantly more time in front of the reinforced object than expected due to chance alone (t7 = 3.134, p =
0.007). There was no detectable side bias with fish roughly spending half their time on each side of divider across both probe trials (right = 0.494; left = 0.506). Maintenance of the operant behavior was both robust and stable. In virtually all trials, fish chose the reinforced image in preference to the non-reinforced one (15/16 p = 0.0006, Fig 3). Of the eight individuals tested, seven consistently preferred the reinforced image between trials, while one individual split trials, 9 choosing the reinforced image in the first trial and the non-reinforced one in the second. Association Time[%]
1 2 3 4 5 6 7 8 Fish
Fig. 3. Successful acquisition of the operant behavior as indicated by association time in probe trials. Vertical bars (N=16) graph the time spent in different areas of the tank for a single probe trial (5-minute) with two trials for each fish (N=8). Stacked bars depict the time spent near the reinforced object [black], non-reinforced object [gray], and the half of the tank away from the screen [white]. Dissociation tests:
Test fish in these trials were more than twice as likely to associate with the object matching the reinforced color over that matching the correct shape (Fig. 4). Individuals spent more time in front of the reinforced color than the reinforced shape (with the results just short of significance in a two-tailed t-test; (t [7] = 1.644, p = 0.070). However, fish selected the object with matching
(i.e. rewarded) color in preference to shape in a significant number of trials (Sign Test [13/16]; p =
0.021). The majority of individuals (5/8) relied to a greater degree on color information in making their choices in both trials, while two individuals preferentially used color in the first 10 trial, and changing to shape in the second. These results indicate that although both cues may be used, color information is dominant over shape.
Individuals spent more time in front of the reinforced color than the reinforced shape with the results just short of significance in a two-tailed t-test; (t [7] = 1.644, p = 0.070). However, fish selected the object with matching (i.e. rewarded) color in preference to shape in a significant number of trials (Sign Test [13/16]; p = 0.021). The majority of individuals (5/8) relied to a greater degree on color information in making their choices in both trials, while two individuals preferentially used color in the first trial, and changing to shape in the second. These results
indicate that although both cues may be used, color information is dominant over shape.
a
a a Association Time[%]
1 2 3 4 5 6 7 8 Fish
Fig. 4 Relative use of color and shape information as indicated by association time in cue- dissociation tests. Vertical bars (N=16) graph the time spent in different areas of the tank for a single dissociation trial (5-minute) with two trials for each fish (N=8). Stacked bars depict the time spent near the reinforced object's color [black], the reinforced object's shape [gray], and the half of the tank away from the screen [white]. 11
There is no evidence of a population side bias (right = 0.555; left = 0.455), nor any indication (from time spent in the ‘no choice’ zone to the rear of the tank), that the fish had particular difficulty with the disassociation task. Initial operant conditioning on square or triangle has no detectable effect on fish response.
DISCUSSION
This study assessed form discrimination and the relative importance of color and shape information in the visual perception of the Malawian cichlid Melanochromis auratus. Consistent with previous work on goldfish and a number of perciformes, M. auratus showed little problem discriminating between colored squares and triangles, despite the artificiality of these symbols.
Overall, our results indicate that by focusing attention on the constituent physical elements of the conditioned images, M. auratus is able to successfully build an association between food reward and the particular object's features. Moreover, the species preferentially relies on color rather than shape as the key feature in the process of object recognition and subsequent recall.
Task acquisition occurred at a similar rate to that in goldfish which required ca. 20–35 days to reach a 75% choice frequency in learning to distinguish between a triangle and a square
(Wyzisk & Neumeyer 2007). In comparison to other cichlids, M. auratus may be slightly faster at mastering detection and discrimination tasks. An unspecified Pseudotropheus sp. needed an average of six sessions to distinguish successfully between a card featuring a square and a blank card in a form discrimination task, and a further 5-15 sessions to discriminate a black triangle and a square (Schluessel et. al., 2012). In that same study, differentiating between a square and a large triangle (again in the absence of color) was the most challenging of several discrimination tasks (including a circle and small triangle), suggesting that the conditioning phase of our experiment might be substantially more efficient if a similarly sized circle would have been used 12 instead of a triangle. The proportion of subjects not meeting criterion in the training phase (3/11;
27%) was consistent with the results found by Agrillo et al (2012) for mosquitofish (Gambusia holbrooki).
Results of the dissociation tests indicate that in M. auratus, the fish’s propensity to use color information takes precedence over shape in the challenge of object recognition. Color as the primary visual feature in object perception within an ecologically-neutral learning paradigm, is consistent with the findings of more naturalistic behavioral experiments. Work on cichlid mate choice has provided evidence that visual cues are of general importance in species recognition of rock-dwelling species from Lake Malawi. Cichlid females use coloration as the main feature in mate choice decisions, even choosing similarly-colored heterospecific males in the absence of conspecific ones (Seehausen & van Alphen, 1998; Couldridge & Alexander, 2002).
A small degree of variability in response (i.e. association time for color or shape), among individuals and between the two dissociation tests was observed. The observed variation was minimal compared to that obtained when information from two features was dissociated in
Xenotoca eiseni, and fish split their responses between geometric and non-geometrically correct features (Sovrano et al., 2003). Some variation between the first and second dissociation tests may derive from the fact that fish remembered the positive stimulus, but also associated the alternative stimulus with negative reinforcement. Upon presentation of the dissociated stimuli fish increasingly approached both previously rewarded stimulus feature, but took time to explore the novel stimuli before stabilizing their choice once more (Schluessel et al., 2012). Finally, because operant variability is what allows a response to adapt to new situations, a response topography with slight variations from one object recognition performance to another (and hence between the two probe trials), was to be expected. Objects in M. auratus’ sensory world consist 13 of combinations of colors and shapes. Given that the waters of Lake Malawi are subject to extensive and continuous changes in underwater visibility (Konings, 2001), the flexibility afforded by the hierarchical use of different visual cues would be favored over absolute reliance on a single object feature. This is evident in the results of behavioral mate choice experiments, which, when color information is obscured by performing experiments under monochromatic light, male pattern and shape differences come into play (Jordan et al., 2003).
Results of the probe trials demonstrate that not only did M. auratus learn to choose the positive stimulus, but also to avoid the negative one. Moreover, there was remarkably little individual variation in strategy. This contrasts rather starkly with the results of what is, to the best of our knowledge, the only other cichlid object recognition study to date. Schluessel et al.
(2012) found Pseudotropheus sp. required between 4-21 sessions before transfer tests, and trial times ranged from 2.0-9.7 seconds in a single test scenario. However, the comparison is an imperfect one perhaps reflecting a difference in methodology (e.g. association time vs % correct choices) rather than any real biological difference.
Results of the dissociation tests clearly indicate that in M. auratus, the fish’s propensity to use color information takes precedence over shape in the challenge of object recognition. Our finding, in an ecologically-neutral learning paradigm, that color is the primary visual feature in object perception, is concordant with the findings of naturalistic behavioral experiments such as mate choice. Behavioral experiments have demonstrated that visual cues are important for species recognition in mbuna (rock-dwelling cichlids from Lake Malawi). Cichlid females use coloration as the main feature in mate choice decisions, even choosing similarly-colored heterospecific males in the absence of conspecific ones (Seehausen & van Alphen, 1998;
Couldridge & Alexander, 2002). 14 A small degree of variability in response (i.e. association time for color or shape), among individuals and between the two dissociation tests was observed. The observed variation was minimal compared to that obtained when information from two features was dissociated in
Xenotoca eiseni and fish split their responses between geometric and non-geometrically correct features (Sovrano et al., 2003). Some variation between the first and second dissociation tests may derive from the fact that fish remembered the positive stimulus, but also associated the alternative stimulus with negative reinforcement. Upon presentation of the dissociated stimuli fish did not automatically continue to approach only the previously rewarded stimulus feature, but took time to explore the novel stimuli before stabilizing their choice once more (Schluessel et al., 2012). Finally, because operant variability is what allows a response to adapt to new situations, response topography with slight variations from one object recognition performance to another (and hence between the two probe trials) was to be expected. Objects in M. auratus’ sensory world consist of combinations of colors and shapes. Given that the waters of Lake
Malawi are subject to extensive and continuous changes in underwater visibility (Konings,
2001), the flexibility afforded by the hierarchical use of different visual cues would be favored over absolute reliance on a single object feature. This is evident in the results of behavioral mate choice experiments, which, when color information is obscured by performing experiments under monochromatic light, male pattern and shape differences come into play (Jordan et al.,
2003).
The experimental design employed here was particularly challenging, because the testing portion of the probe trials was 10 times longer than the maximum wait time to reward during training. Despite this, fish still spent a significantly greater amount of time in front of their conditioned image, supporting both the efficacy of the operant conditioning and the stability of 15 M. auratus’ choices. Association time has traditionally been employed to evaluate social preference and mate choice in fish (Buckingham et al 2007; Fisher & Rosenthal 2006), but it has also proven to be an efficient measure of visual discrimination here. Agrillo et al (2012) recently tested a similar method by replicating published experiments on numerical abilities of mosquitofish, and their study confirms the efficiency advantage of a continuous measure of association with a reinforced stimulus during one or a few probe trials, rather than computing the proportion of correct choices across many consecutive probe trials.
Acts of discrimination rely on a variety of complex neurological factors (central and peripheral), which are rather poorly understood for cichlids (e.g. color, luminance, edges).
Behavioral assays such as the optomotor response are being used to assess these neurological factors (Smith et al 2011; Didion et al, in prep), and it is conceivable that new methodologies could be deployed to explore feature-specific sensory processes equivalent to those found in humans (McGinnis & Keil 2011). It is clear though, that an animal’s propensity to use a particular object feature as a basis for choice is frequently determined by the extent to which the features are discriminable. Although we do not know that color and shape are equally discriminable in cichlids, the very simplicity of the color and shape combinations employed here provide a clear ranking of object features in the well-defined case. More challenging choice scenarios would, however, demand enhanced quantification and calibration of feature dimensions. Important future directions would include testing whether color is consistently the primary visual component used in the object recognition of more natural (possibly vital) stimuli, and under scotopic or mesopic conditions.
The features employed by cichlids in the task tested here viz., trying to recognize a previously learned object, are relatively simple low-level representations. Although it is likely 16 that the choices a cichlid must adjudicate outside the experimental setting are based on high-level semantic properties, we have demonstrated a clear precedence of color over shape information under photopic conditions. Additionally, we show that individual differences in the relative use of color and shape information are remarkably modest.
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