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The effect of motion aftereffect on optomotor response in larva and adult zebrafish
ARTICLE IN PRESS
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Neuroscience Letters xxx (2013) xxx–xxx
Contents lists available at SciVerse ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
The effect of motion aftereffect on optomotor response in larva and adult zebrafish
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M. Najafian, N. Alerasool., J. Moshtaghian ∗ Department of Biology, University of Isfahan, Isfahan, Iran
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h i g h l i g h t s • • • •
Existence of motion aftereffect (MAE) was investigated in zebrafish. Simple gratings were shown to zebrafish in order to induce optomotor response. Adult zebrafish’s behavior significantly was affected by the grating in test group. Further studies are required to establish or refute presence of MAE in larval zebrafish.
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Article history: Received 1 April 2013 Received in revised form 23 May 2013 Accepted 25 May 2013
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Keywords: Zebrafish OMR Motion aftereffect Visual illusion Motion perception
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1. Introduction
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Motion aftereffect (MAE) occurs after presenting a moving stimulus to fixed subjects, as an apparent MAE the subject moves in the opposite direction. This natural process provides an excellent tool to investigate visual motion perception. Zebrafish is an important animal model with an extensive molecular toolkit, but there is a lack of the comparative understanding of its perceptual processes. This study was designed to study the optomotor response (OMR), in which the fish swims in the same direction of a moving stimulus in both adult and larvae zebrafish. Simple square wave gratings moving in a specific horizontal direction (with a precise visual angle) were shown to a test group. After an adaptation phase, a static grating was shown for a short period during which the movement of the fish was recorded. In the control group, the same procedure was applied but the grating pattern was shown moving randomly back and forth followed by a static grating. Time spent swimming in either the same or the opposite direction of the adaptation grating was recorded as line index (LI) and non-line index (NI). The results indicate that NI was more than LI for the test group, while there was no significant difference between NI and LI in the control group. These results suggest that MAE occurs in zebrafish causing OMR. © 2013 Published by Elsevier Ireland Ltd.
All throughout life, inputs from a combination of senses are received and analyzed to better perceive and in turn react to the surrounding environment. Of all our senses, sight is of particular importance and yet many of its complexities remain unrevealed. Innumerable details of each scene are constantly received but how these details are interpreted is still an open question in visual perception. A fascinating area in vision sciences seeks to better understand how visual perception could arise from neurological processes. Many studies have been done to better understand how perceptual groupings could be originated from the interactions of different cells [10,17].
∗ Corresponding author at: Department of Biology, University of Isfahan, Hezarjarib Avenue, Isfahan 81746-73441, Iran. Tel.:+98 311 7932465; fax: +98 311 7932456. E-mail addresses: [email protected], mnajafi[email protected] (J. Moshtaghian).
Visual illusions, misinterpretations of incoming sensory information by the brain, are often used to tackle the most interesting problems of perception. Another way of interpreting these illusions is to think of them as the manner, in which, the nervous system has evolved to handle specific stimuli that are common in the natural living environment of the animals. Thus, by studying different visual illusions, we can learn about different visual pathways and the processes that underlie these phenomena. Studies of visual illusions have made possible a better understanding of the neurobiology of vision and at the same time have paved the way to new experiments and possibilities for research in systems neuroscience [8,10,28]. Although the visual sensory system plays a vital role in making sense of the natural environment as a basic function for creating secondary behavior, the process of how the brain takes various inputs and generates meaningful outputs in such forms as locomotion, learning, and memory is still poorly understood. Various biological principles of perception have been extracted from studying different visual illusions in humans and other species. An example is the elegant study by Nieder and Wagnerin in which they
0304-3940/$ – see front matter © 2013 Published by Elsevier Ireland Ltd. http://dx.doi.org/10.1016/j.neulet.2013.05.072
Please cite this article in press as: M. Najafian, et al., The effect of motion aftereffect on optomotor response in larva and adult zebrafish, Neurosci. Lett. (2013), http://dx.doi.org/10.1016/j.neulet.2013.05.072
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determined that “owls can see illusory contours and they perceive this illusion in the same way which we do” [27]. Motion aftereffect (MAE) is a well-known and ancient visual illu60 sion that has been well studied in visual perception literature. It 61 occurs after viewing a moving stimulus as an apparent movement 62 in the opposite direction. It was first reported by Aristotle and is 63 considered to be caused by opponent processing, which explains 64 these kinds of illusions according to the existence of competing 65 neural populations in a balance of tonic activity. “According to this 66 view, a subpopulation can be ‘fatigued’, and another subpopulation 67 can dominate the push–pull competition and briefly control the 68 perception” [10]. Neuroscience literatures has long established the 69 effects of MAE in primates [1]. Also it has been reported in several 70 studies that aftereffect adaptation occurs in different cortical sites 71 of visual cortex, which only exists in primates and mammals [6,23]. 72 MAE studies have had a central role in understanding and devel73 oping theories on motion perception and its neural circuits in the 74 brain. Simple neural explanation of MAE was primarily advocated 75 by Sutherland, who was inspired by Hubel and Wiesel’s discovery 76 of direction-selective cortical cells in cats. The direction of a mov77 ing object might depend on the ratio of firing in neural cells that 78 are sensitive to different motion direction. After prolonged move79 ment in one direction, presentation of a stationary image would 80 produce a lower firing rate in cells that had just been stimulated, 81 thus movement in the opposite direction would appear to occur 82 [23,34]. 83 The adaptation in the motion-selective cells in the primary 84 visual cortex is the common view of MAE and has been verified 85 in a variety of animals including cats [19], rabbits [34], macaques 86 [20] and flies [26], specifying several visual cortical sites that are 87 involved in the process of MAE. New studies have also revealed 88 that MAE may operate at several levels of the motion detection 89 pathways through mechanisms located pre-synaptic to motion90 sensitive sites [23,26]. Besides, adaptation has been described as 91 a form of gain of control that exploits the efficiency of the spread 92 of information at multiple levels of the visual pathway [15,23,26]. 93 Furthermore, MAE is tuned both by temporal and spatial frequen94 cies [1,2,37]. For example, in the case of spatial frequency, “the 95 strongest effect of the illusion is created when the adapting grating 96 and the stationary test grating have the same spatial frequencies 97 and for temporal frequency, the strongest effect has been reported 98 in a specific frequency for each of the species studied” [32]. 99 In this study, zebrafish was used as an animal model to inves100 tigate the effect of MAE. Zebrafish has been an effective animal 101 model in different fields of biological sciences throughout the years. 102 Among other animal models, they have been a suitable choice 103 in developmental neuroscience investigations. One of the most 104 important reasons that has made this organism a valuable model 105 in vision science is the similarity of its visual system to that of 106 other vertebrates. There are some other important characteris107 tics of zebrafish to be mentioned. Firstly, they breed in abundant 108 numbers and eggs are laid regularly. Secondly, their developmen109 tal processes are rapid and they get to maturity within 3 months 110 Q2 [4–2]. In addition, as an emphasis on visual analysis, zebrafish is 111 the ideal animal model for its visual system develops rapidly dur112 ing the larval stage. This might be due to the fact that vision is 113 required in both avoiding predators and capturing food. Zebrafish 114 show signs of visual behavior and capture prey at 5 days post fertil115 ization (dpf) [14]. “The adult zebrafish brain is only about 4.5 mm 116 long and between 0.4 and 2 mm thick and the larval brain at 5 dpf 117 is less than 500 mm thick and 1.5 mm long; making virtually all 118 neurons accessible to multi photon microscopy in vivo” [14,15]. 119 Optomotor response (OMR), a commonly studied visual behav120 ior in zebrafish, is observed as swimming in the direction of moving 121 visual stimuli. It is probably a way to reduce any ‘slippage’ of the 122 visual surroundings on the retina and could be induced by a moving 123 58 59
repetitive stimulus pattern in the environment. This behavior is a valuable paradigm that is mostly used for studying visual system functions. In most studies this pattern consists of vertical stripes, which may be in black and white, different gray contrasts or in color. In general, the accessory optic area (AOS), the pre-tectal complex (PTC), and the tectum opticum (TO) appear to interact with motor areas of the fish. This behavior is also considered to be mediated by red and green cones [22,26,31]. In order to evoke OMR in larvae, computer animated grating is usually presented underneath or beside the chamber where zebrafish are placed and it is observed that they swim in the direction of moving stripes. This behavior is commonly observed at 7 dpf and can also be applied in adult zebrafish [14,17,26]. Zebrafish show a strong OMR that may be stimulated mechanically. OMR can potentially be used to investigate complex visual phenomena such as motion perception in zebrafish. Zebrafish have been providing clues into better understanding the formation and function of visual sensory circuits in an organism [18,25,26]. However, there is not much information available on MAE in zebrafish in the literature and the present study was designed to investigate such behavior in this animal.
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2. Materials and methods
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120 six-month-old male and female adult zebrafish were used in this experiment. The fish were purchased from a local pet store. In order to start conditioning procedures in a new environment, they were accommodated in an aquarium housing system two weeks prior to the test sessions. All subjects were approximately the same size [29,21,30,35]. The fish were housed in two separate 300-mm long plexiglass tanks, each containing 60 adults, one maintaining the test subjects and the other as the control group. The water temperature was kept between 28 and 30 ◦ C, a pH range between 6.8 and 7.0 was maintained and a light cycle of 14 h on and 10 h off was provided [29,12,24]. Fish were fed twice daily with flake fish food containing frozen and live brine shrimp [5,6,4]. All experiments described here were carried out between 1 pm and 6 pm. The fish were housed individually for at least 30 min in order to get naturally schooling fish accustomed to being alone and to provide a means of identifying each fish. The fish were able to swim back and forth in the test tanks, 10–20 mm away from the screen [4,35]. 2.2. Larvae Larvae were bred from crosses of the wild type adult zebrafish. They were raised on a 14:10 h light–dark cycle and the lights were on at 8 am daily. Behavioral testing always took place between 1 pm and 6 pm on day 7 of post fertilization. For each experiment, a shallow 300 mm long plexiglass tank containing approximately 50 larvae was placed in front of the monitor screen and adaptation index (AI) was then measured [23,38] (Fig. 1). 2.3. Movie design and presentation Movies were created using MATLAB and Psychophysics Toolbox Version 3 (PTB-3 Mario Kleiner, David Brainard 2007). Movies were displayed using a flat LCD monitor located behind the test tank [29,11,30]. Each movie contained two phases. The first phase was a 2-min adaptation phase containing rightward or leftward simple gratings with 30 horizontal degrees, temporal frequency of 0.93 Hz and spatial frequency of 0.08 cycle/degree. During the adaptation phase fish were swimming in the direction of the moving grating as a result of optomotor response [29,22,30,37]. For the second phase, a static grating was displayed for 20 s during which
Please cite this article in press as: M. Najafian, et al., The effect of motion aftereffect on optomotor response in larva and adult zebrafish, Neurosci. Lett. (2013), http://dx.doi.org/10.1016/j.neulet.2013.05.072
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Fig. 1. one frame of test grating.
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a Camileo HD Toshiba video camera fixed on top of the test tank to record the movement of the fish. During the adaptation phase of the control group, the same grating pattern was shown but moving bi-directionally where the grating moves back and forth with a random frequency followed by the same static grating and the movements of fish were recorded. For the test group, the distance spent swimming to either the same or in the opposite direction of the grating was calculated as line and non-line indices (LI and NI). The differences between these two figures were noted as an adaptation index (AI). A negative response was described as movement of fish in the direction of the grating and a positive response was described as movement opposing the direction of the moving grating, then the responses were normalized to the maximum. As for the control group, random right or left directions were chosen as preference. Then the distance traveled by the fish in either alongside or opposite to the specified direction was calculated as line and non-line indices (LI and NI). Other procedures were the same as for the test group [23]. Two-way analysis of variance (ANOVA) was used to analyze the data. Bonferroni post hoc test was performed to compare the test and the control groups. Data are indicated as mean ± SEM. A p-value of less than 5% was considered statistically significant. For analyzing recorded movies, ImageJ and MATLAB Tool for Digitalizing Video Files and Calibrating Camera were used [29,30]. The distance each fish spent swimming along or opposing the moving grating was obtained and their differences were measured as the AI for each fish. This process was done for each single fish in the test and the control groups and the results were then normalized.
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3. Results
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Sixty adult fish for either of the test or the control groups were used. The distance each fish swam either in the same direction or in the opposite direction of the moving grating was measured and were normalized according to their AI. As indicated in Fig. 2, the
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Adaptation index
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-0.2 Fig. 2. Adaptation index in adult and larva zebrafish after motion after effect challenge.
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two-way ANOVA of the data revealed that MAE had a significant effect on AI in adult zebrafish (F(1,176) = 5.9, p = 0.0162). Bonferroni analysis between the test and the control groups in adult zebrafish indicated that AI in the test group was significantly more than the controls. The p-value for adult zebrafish was less than 0.01 (t = 3.402) presenting a significant difference between the test and the control groups of adult zebrafish indicating that the null hypothesis can be rejected (p < 0.01). This means that zebrafish in the test group swam significantly more frequently in the opposite direction of moving grating in the test phase compared to the control group. High AI in the test group means that fish were adapted to the direction of moving grating. It also indicates that motion aftereffect can have an effect on visual behavior in adult zebrafish. The same experiment was carried out for zebrafish larvae in order to find different effects of MAE in the larvae and the adults visual behavior. Furthermore, A Z-test was performed to compare the mean AI of the test and control zebrafish larvae. The results indicated no statistically significant difference in either test (p = 0.30) or control (p = 0.44) group as indicated in Fig. 2 (t = 0.467, p > 0.05).
4. Discussion Zebrafish are a widely used animal model in circuit and visual neuroscience. Calcium imaging and laser ablation methods have been used to discover different neural circuits in adult and larval zebrafish. These studies identified small groups of descending hindbrain neurons that are correlated with performing visually evoked swimming patterns. Other experiments have demonstrated that motor neurons and pre-motor neurons are located in the spinal cord and optic tectum of zebrafish. Moreover, zebrafish can perceive second-order motion and colors, a computation that in mammals is usually characterized in the visual cortex [7,15]. On the other hand, unilateral ablation in tectal neurons of adult zebrafish, demonstrated that tectal neurons are not only responsible for input from both eyes but their receptive fields and direction selectivity are clearly correlated. It has been suggested that visual inputs from both eyes can be integrated into a common motion direction signal at this stage [15]. Additionally, rapid development of the visual system in larval zebrafish along with the size dominance of the eyes relative to other body structures suggests the importance of the visual system for the larvae [10,16]. “The larvae zebrafish retina in 5 dpf consists of the entire cell types of vertebrate retinas; while rod photoreceptors are morphologically detectable in the retina, they contribute to vision after 15 dpf, but they do not become like adult rods until 30 dpf [13,14,16]”. Motor behavior in larval zebrafish such as directed escape movement, simple swimming, prey capture, OMR and OKR develope approximately between 18 h post-fertilization (hpf) and 9 dpf [15,21]. Congruently, using stimuli targeting specific cone types has indicated that a luminance channel, which contains Land M-cone signals, dominates motion detection in zebrafish. Also, short-wavelength cones seem not to contribute to OMR, instead provide a major input to another visual behavior in zebrafish called phototaxis [29]. In this study, a simple psychophysical test was used to explore whether or not the OMR of zebrafish can be affected by MAE. A feature of motion investigated here, as an adaptation factor, was the Fourier motion energy, which the fish can perceive from the environment [23,25,35,36]. The results of this study suggest that MAE has the potential to be used in investigating visual motion processing circuits in adult zebrafish as it has been done in primates for decades with great results. But unlike adult zebrafish, a significant difference in response to MAE in larval zebrafish was not observed between test and control group.
Please cite this article in press as: M. Najafian, et al., The effect of motion aftereffect on optomotor response in larva and adult zebrafish, Neurosci. Lett. (2013), http://dx.doi.org/10.1016/j.neulet.2013.05.072
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5. Conclusion
The difference observed between adult and larvae may be explained by the developmental alterations causing the motion 281 processing circuits to mature. As a by-product, these changes in 282 a way enable the MAE, similar to a primate brain. Furthermore, 283 the state of variance between adult and larvae may have resulted 284 from the different developmental processes involved in cone and 285 rod photoreceptors along with the tasks that each photoreceptor 286 undertakes in OMR. In zebrafish, behavior also depends on different 287 color channels developed independently during larvae develop288 ment. Therefore, quantitative behavioral studies in combination 289 with laser ablations for mapping visual behaviors to different target 290 areas of retinal ganglion cells could be used in order to find differ291 ences between larval and adult zebrafish behavior in the perception 292 of second-order motion. 293 Prospect research using techniques such as rolling tools could 294 be used for investigating the longer effects of motion adaptation 295 in adult zebrafish. Alternatively, the fish can be fixed in posi296 tion as an optokinetic response of the fish is then being recorded 297 for measuring motion adaptation in zebrafish. Some studies have 298 demonstrated that OMR in zebrafish has temporal characteristic of 299 a low-pass filter when the spatial frequency are low and of a band300 pass filter when the spatial frequencies are high. “For example it 301 has been proved that zebrafish show the OMR over a wide range 302 of velocities (up to 1030◦ /s) and of temporal frequencies (up to 303 256 cps) [22]”. MAEs, on the other hand, are controlled by a sin304 gle low-pass temporal frequency mechanism and by a series of 305 Q3 band-pass spatial frequency mechanisms [44]. As a final note, in 306 this study, the spatial and temporal frequencies of the grating were 307 chosen to evoke the long and effective optomotor response in adult 308 and larvae, but in future studies different frequencies can be used 309 for evoking OMR in order to find out whether or not MAE with a 310 defined range of temporal and spatial frequencies of gratings can 311 affect OMR. 312 280
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Uncited references [3,9,33]. Acknowledgments
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The authors would like to appreciate Prof. Stuart Anstis and Prof. Patrick Cavanagh for their kind revisions and their countless comments on the manuscript. They would also like to thank Dr. Ali Moeeny and Mohammad Goudarzi for their constructive support during the experiment.
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Please cite this article in press as: M. Najafian, et al., The effect of motion aftereffect on optomotor response in larva and adult zebrafish, Neurosci. Lett. (2013), http://dx.doi.org/10.1016/j.neulet.2013.05.072
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G Model NSL 29828 1–4
Neuroscience Letters xxx (2013) xxx–xxx
Contents lists available at SciVerse ScienceDirect
Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
The effect of motion aftereffect on optomotor response in larva and adult zebrafish
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M. Najafian, N. Alerasool., J. Moshtaghian ∗ Department of Biology, University of Isfahan, Isfahan, Iran
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h i g h l i g h t s • • • •
Existence of motion aftereffect (MAE) was investigated in zebrafish. Simple gratings were shown to zebrafish in order to induce optomotor response. Adult zebrafish’s behavior significantly was affected by the grating in test group. Further studies are required to establish or refute presence of MAE in larval zebrafish.
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Article history: Received 1 April 2013 Received in revised form 23 May 2013 Accepted 25 May 2013
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Keywords: Zebrafish OMR Motion aftereffect Visual illusion Motion perception
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1. Introduction
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Motion aftereffect (MAE) occurs after presenting a moving stimulus to fixed subjects, as an apparent MAE the subject moves in the opposite direction. This natural process provides an excellent tool to investigate visual motion perception. Zebrafish is an important animal model with an extensive molecular toolkit, but there is a lack of the comparative understanding of its perceptual processes. This study was designed to study the optomotor response (OMR), in which the fish swims in the same direction of a moving stimulus in both adult and larvae zebrafish. Simple square wave gratings moving in a specific horizontal direction (with a precise visual angle) were shown to a test group. After an adaptation phase, a static grating was shown for a short period during which the movement of the fish was recorded. In the control group, the same procedure was applied but the grating pattern was shown moving randomly back and forth followed by a static grating. Time spent swimming in either the same or the opposite direction of the adaptation grating was recorded as line index (LI) and non-line index (NI). The results indicate that NI was more than LI for the test group, while there was no significant difference between NI and LI in the control group. These results suggest that MAE occurs in zebrafish causing OMR. © 2013 Published by Elsevier Ireland Ltd.
All throughout life, inputs from a combination of senses are received and analyzed to better perceive and in turn react to the surrounding environment. Of all our senses, sight is of particular importance and yet many of its complexities remain unrevealed. Innumerable details of each scene are constantly received but how these details are interpreted is still an open question in visual perception. A fascinating area in vision sciences seeks to better understand how visual perception could arise from neurological processes. Many studies have been done to better understand how perceptual groupings could be originated from the interactions of different cells [10,17].
∗ Corresponding author at: Department of Biology, University of Isfahan, Hezarjarib Avenue, Isfahan 81746-73441, Iran. Tel.:+98 311 7932465; fax: +98 311 7932456. E-mail addresses: [email protected], mnajafi[email protected] (J. Moshtaghian).
Visual illusions, misinterpretations of incoming sensory information by the brain, are often used to tackle the most interesting problems of perception. Another way of interpreting these illusions is to think of them as the manner, in which, the nervous system has evolved to handle specific stimuli that are common in the natural living environment of the animals. Thus, by studying different visual illusions, we can learn about different visual pathways and the processes that underlie these phenomena. Studies of visual illusions have made possible a better understanding of the neurobiology of vision and at the same time have paved the way to new experiments and possibilities for research in systems neuroscience [8,10,28]. Although the visual sensory system plays a vital role in making sense of the natural environment as a basic function for creating secondary behavior, the process of how the brain takes various inputs and generates meaningful outputs in such forms as locomotion, learning, and memory is still poorly understood. Various biological principles of perception have been extracted from studying different visual illusions in humans and other species. An example is the elegant study by Nieder and Wagnerin in which they
0304-3940/$ – see front matter © 2013 Published by Elsevier Ireland Ltd. http://dx.doi.org/10.1016/j.neulet.2013.05.072
Please cite this article in press as: M. Najafian, et al., The effect of motion aftereffect on optomotor response in larva and adult zebrafish, Neurosci. Lett. (2013), http://dx.doi.org/10.1016/j.neulet.2013.05.072
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determined that “owls can see illusory contours and they perceive this illusion in the same way which we do” [27]. Motion aftereffect (MAE) is a well-known and ancient visual illu60 sion that has been well studied in visual perception literature. It 61 occurs after viewing a moving stimulus as an apparent movement 62 in the opposite direction. It was first reported by Aristotle and is 63 considered to be caused by opponent processing, which explains 64 these kinds of illusions according to the existence of competing 65 neural populations in a balance of tonic activity. “According to this 66 view, a subpopulation can be ‘fatigued’, and another subpopulation 67 can dominate the push–pull competition and briefly control the 68 perception” [10]. Neuroscience literatures has long established the 69 effects of MAE in primates [1]. Also it has been reported in several 70 studies that aftereffect adaptation occurs in different cortical sites 71 of visual cortex, which only exists in primates and mammals [6,23]. 72 MAE studies have had a central role in understanding and devel73 oping theories on motion perception and its neural circuits in the 74 brain. Simple neural explanation of MAE was primarily advocated 75 by Sutherland, who was inspired by Hubel and Wiesel’s discovery 76 of direction-selective cortical cells in cats. The direction of a mov77 ing object might depend on the ratio of firing in neural cells that 78 are sensitive to different motion direction. After prolonged move79 ment in one direction, presentation of a stationary image would 80 produce a lower firing rate in cells that had just been stimulated, 81 thus movement in the opposite direction would appear to occur 82 [23,34]. 83 The adaptation in the motion-selective cells in the primary 84 visual cortex is the common view of MAE and has been verified 85 in a variety of animals including cats [19], rabbits [34], macaques 86 [20] and flies [26], specifying several visual cortical sites that are 87 involved in the process of MAE. New studies have also revealed 88 that MAE may operate at several levels of the motion detection 89 pathways through mechanisms located pre-synaptic to motion90 sensitive sites [23,26]. Besides, adaptation has been described as 91 a form of gain of control that exploits the efficiency of the spread 92 of information at multiple levels of the visual pathway [15,23,26]. 93 Furthermore, MAE is tuned both by temporal and spatial frequen94 cies [1,2,37]. For example, in the case of spatial frequency, “the 95 strongest effect of the illusion is created when the adapting grating 96 and the stationary test grating have the same spatial frequencies 97 and for temporal frequency, the strongest effect has been reported 98 in a specific frequency for each of the species studied” [32]. 99 In this study, zebrafish was used as an animal model to inves100 tigate the effect of MAE. Zebrafish has been an effective animal 101 model in different fields of biological sciences throughout the years. 102 Among other animal models, they have been a suitable choice 103 in developmental neuroscience investigations. One of the most 104 important reasons that has made this organism a valuable model 105 in vision science is the similarity of its visual system to that of 106 other vertebrates. There are some other important characteris107 tics of zebrafish to be mentioned. Firstly, they breed in abundant 108 numbers and eggs are laid regularly. Secondly, their developmen109 tal processes are rapid and they get to maturity within 3 months 110 Q2 [4–2]. In addition, as an emphasis on visual analysis, zebrafish is 111 the ideal animal model for its visual system develops rapidly dur112 ing the larval stage. This might be due to the fact that vision is 113 required in both avoiding predators and capturing food. Zebrafish 114 show signs of visual behavior and capture prey at 5 days post fertil115 ization (dpf) [14]. “The adult zebrafish brain is only about 4.5 mm 116 long and between 0.4 and 2 mm thick and the larval brain at 5 dpf 117 is less than 500 mm thick and 1.5 mm long; making virtually all 118 neurons accessible to multi photon microscopy in vivo” [14,15]. 119 Optomotor response (OMR), a commonly studied visual behav120 ior in zebrafish, is observed as swimming in the direction of moving 121 visual stimuli. It is probably a way to reduce any ‘slippage’ of the 122 visual surroundings on the retina and could be induced by a moving 123 58 59
repetitive stimulus pattern in the environment. This behavior is a valuable paradigm that is mostly used for studying visual system functions. In most studies this pattern consists of vertical stripes, which may be in black and white, different gray contrasts or in color. In general, the accessory optic area (AOS), the pre-tectal complex (PTC), and the tectum opticum (TO) appear to interact with motor areas of the fish. This behavior is also considered to be mediated by red and green cones [22,26,31]. In order to evoke OMR in larvae, computer animated grating is usually presented underneath or beside the chamber where zebrafish are placed and it is observed that they swim in the direction of moving stripes. This behavior is commonly observed at 7 dpf and can also be applied in adult zebrafish [14,17,26]. Zebrafish show a strong OMR that may be stimulated mechanically. OMR can potentially be used to investigate complex visual phenomena such as motion perception in zebrafish. Zebrafish have been providing clues into better understanding the formation and function of visual sensory circuits in an organism [18,25,26]. However, there is not much information available on MAE in zebrafish in the literature and the present study was designed to investigate such behavior in this animal.
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2. Materials and methods
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120 six-month-old male and female adult zebrafish were used in this experiment. The fish were purchased from a local pet store. In order to start conditioning procedures in a new environment, they were accommodated in an aquarium housing system two weeks prior to the test sessions. All subjects were approximately the same size [29,21,30,35]. The fish were housed in two separate 300-mm long plexiglass tanks, each containing 60 adults, one maintaining the test subjects and the other as the control group. The water temperature was kept between 28 and 30 ◦ C, a pH range between 6.8 and 7.0 was maintained and a light cycle of 14 h on and 10 h off was provided [29,12,24]. Fish were fed twice daily with flake fish food containing frozen and live brine shrimp [5,6,4]. All experiments described here were carried out between 1 pm and 6 pm. The fish were housed individually for at least 30 min in order to get naturally schooling fish accustomed to being alone and to provide a means of identifying each fish. The fish were able to swim back and forth in the test tanks, 10–20 mm away from the screen [4,35]. 2.2. Larvae Larvae were bred from crosses of the wild type adult zebrafish. They were raised on a 14:10 h light–dark cycle and the lights were on at 8 am daily. Behavioral testing always took place between 1 pm and 6 pm on day 7 of post fertilization. For each experiment, a shallow 300 mm long plexiglass tank containing approximately 50 larvae was placed in front of the monitor screen and adaptation index (AI) was then measured [23,38] (Fig. 1). 2.3. Movie design and presentation Movies were created using MATLAB and Psychophysics Toolbox Version 3 (PTB-3 Mario Kleiner, David Brainard 2007). Movies were displayed using a flat LCD monitor located behind the test tank [29,11,30]. Each movie contained two phases. The first phase was a 2-min adaptation phase containing rightward or leftward simple gratings with 30 horizontal degrees, temporal frequency of 0.93 Hz and spatial frequency of 0.08 cycle/degree. During the adaptation phase fish were swimming in the direction of the moving grating as a result of optomotor response [29,22,30,37]. For the second phase, a static grating was displayed for 20 s during which
Please cite this article in press as: M. Najafian, et al., The effect of motion aftereffect on optomotor response in larva and adult zebrafish, Neurosci. Lett. (2013), http://dx.doi.org/10.1016/j.neulet.2013.05.072
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Fig. 1. one frame of test grating.
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a Camileo HD Toshiba video camera fixed on top of the test tank to record the movement of the fish. During the adaptation phase of the control group, the same grating pattern was shown but moving bi-directionally where the grating moves back and forth with a random frequency followed by the same static grating and the movements of fish were recorded. For the test group, the distance spent swimming to either the same or in the opposite direction of the grating was calculated as line and non-line indices (LI and NI). The differences between these two figures were noted as an adaptation index (AI). A negative response was described as movement of fish in the direction of the grating and a positive response was described as movement opposing the direction of the moving grating, then the responses were normalized to the maximum. As for the control group, random right or left directions were chosen as preference. Then the distance traveled by the fish in either alongside or opposite to the specified direction was calculated as line and non-line indices (LI and NI). Other procedures were the same as for the test group [23]. Two-way analysis of variance (ANOVA) was used to analyze the data. Bonferroni post hoc test was performed to compare the test and the control groups. Data are indicated as mean ± SEM. A p-value of less than 5% was considered statistically significant. For analyzing recorded movies, ImageJ and MATLAB Tool for Digitalizing Video Files and Calibrating Camera were used [29,30]. The distance each fish spent swimming along or opposing the moving grating was obtained and their differences were measured as the AI for each fish. This process was done for each single fish in the test and the control groups and the results were then normalized.
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3. Results
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Sixty adult fish for either of the test or the control groups were used. The distance each fish swam either in the same direction or in the opposite direction of the moving grating was measured and were normalized according to their AI. As indicated in Fig. 2, the
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-0.2 Fig. 2. Adaptation index in adult and larva zebrafish after motion after effect challenge.
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two-way ANOVA of the data revealed that MAE had a significant effect on AI in adult zebrafish (F(1,176) = 5.9, p = 0.0162). Bonferroni analysis between the test and the control groups in adult zebrafish indicated that AI in the test group was significantly more than the controls. The p-value for adult zebrafish was less than 0.01 (t = 3.402) presenting a significant difference between the test and the control groups of adult zebrafish indicating that the null hypothesis can be rejected (p < 0.01). This means that zebrafish in the test group swam significantly more frequently in the opposite direction of moving grating in the test phase compared to the control group. High AI in the test group means that fish were adapted to the direction of moving grating. It also indicates that motion aftereffect can have an effect on visual behavior in adult zebrafish. The same experiment was carried out for zebrafish larvae in order to find different effects of MAE in the larvae and the adults visual behavior. Furthermore, A Z-test was performed to compare the mean AI of the test and control zebrafish larvae. The results indicated no statistically significant difference in either test (p = 0.30) or control (p = 0.44) group as indicated in Fig. 2 (t = 0.467, p > 0.05).
4. Discussion Zebrafish are a widely used animal model in circuit and visual neuroscience. Calcium imaging and laser ablation methods have been used to discover different neural circuits in adult and larval zebrafish. These studies identified small groups of descending hindbrain neurons that are correlated with performing visually evoked swimming patterns. Other experiments have demonstrated that motor neurons and pre-motor neurons are located in the spinal cord and optic tectum of zebrafish. Moreover, zebrafish can perceive second-order motion and colors, a computation that in mammals is usually characterized in the visual cortex [7,15]. On the other hand, unilateral ablation in tectal neurons of adult zebrafish, demonstrated that tectal neurons are not only responsible for input from both eyes but their receptive fields and direction selectivity are clearly correlated. It has been suggested that visual inputs from both eyes can be integrated into a common motion direction signal at this stage [15]. Additionally, rapid development of the visual system in larval zebrafish along with the size dominance of the eyes relative to other body structures suggests the importance of the visual system for the larvae [10,16]. “The larvae zebrafish retina in 5 dpf consists of the entire cell types of vertebrate retinas; while rod photoreceptors are morphologically detectable in the retina, they contribute to vision after 15 dpf, but they do not become like adult rods until 30 dpf [13,14,16]”. Motor behavior in larval zebrafish such as directed escape movement, simple swimming, prey capture, OMR and OKR develope approximately between 18 h post-fertilization (hpf) and 9 dpf [15,21]. Congruently, using stimuli targeting specific cone types has indicated that a luminance channel, which contains Land M-cone signals, dominates motion detection in zebrafish. Also, short-wavelength cones seem not to contribute to OMR, instead provide a major input to another visual behavior in zebrafish called phototaxis [29]. In this study, a simple psychophysical test was used to explore whether or not the OMR of zebrafish can be affected by MAE. A feature of motion investigated here, as an adaptation factor, was the Fourier motion energy, which the fish can perceive from the environment [23,25,35,36]. The results of this study suggest that MAE has the potential to be used in investigating visual motion processing circuits in adult zebrafish as it has been done in primates for decades with great results. But unlike adult zebrafish, a significant difference in response to MAE in larval zebrafish was not observed between test and control group.
Please cite this article in press as: M. Najafian, et al., The effect of motion aftereffect on optomotor response in larva and adult zebrafish, Neurosci. Lett. (2013), http://dx.doi.org/10.1016/j.neulet.2013.05.072
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5. Conclusion
The difference observed between adult and larvae may be explained by the developmental alterations causing the motion 281 processing circuits to mature. As a by-product, these changes in 282 a way enable the MAE, similar to a primate brain. Furthermore, 283 the state of variance between adult and larvae may have resulted 284 from the different developmental processes involved in cone and 285 rod photoreceptors along with the tasks that each photoreceptor 286 undertakes in OMR. In zebrafish, behavior also depends on different 287 color channels developed independently during larvae develop288 ment. Therefore, quantitative behavioral studies in combination 289 with laser ablations for mapping visual behaviors to different target 290 areas of retinal ganglion cells could be used in order to find differ291 ences between larval and adult zebrafish behavior in the perception 292 of second-order motion. 293 Prospect research using techniques such as rolling tools could 294 be used for investigating the longer effects of motion adaptation 295 in adult zebrafish. Alternatively, the fish can be fixed in posi296 tion as an optokinetic response of the fish is then being recorded 297 for measuring motion adaptation in zebrafish. Some studies have 298 demonstrated that OMR in zebrafish has temporal characteristic of 299 a low-pass filter when the spatial frequency are low and of a band300 pass filter when the spatial frequencies are high. “For example it 301 has been proved that zebrafish show the OMR over a wide range 302 of velocities (up to 1030◦ /s) and of temporal frequencies (up to 303 256 cps) [22]”. MAEs, on the other hand, are controlled by a sin304 gle low-pass temporal frequency mechanism and by a series of 305 Q3 band-pass spatial frequency mechanisms [44]. As a final note, in 306 this study, the spatial and temporal frequencies of the grating were 307 chosen to evoke the long and effective optomotor response in adult 308 and larvae, but in future studies different frequencies can be used 309 for evoking OMR in order to find out whether or not MAE with a 310 defined range of temporal and spatial frequencies of gratings can 311 affect OMR. 312 280
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Uncited references [3,9,33]. Acknowledgments
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The authors would like to appreciate Prof. Stuart Anstis and Prof. Patrick Cavanagh for their kind revisions and their countless comments on the manuscript. They would also like to thank Dr. Ali Moeeny and Mohammad Goudarzi for their constructive support during the experiment.
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Please cite this article in press as: M. Najafian, et al., The effect of motion aftereffect on optomotor response in larva and adult zebrafish, Neurosci. Lett. (2013), http://dx.doi.org/10.1016/j.neulet.2013.05.072
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