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Head movements and depth perception
Behavioural Processes 64 (2003) 17–19
Mini-review
Head movements and depth perception夽 Martina Wicklein Computational Neurobiology Laboratory, Howard Hughes Medical Institute, Salk Institute, 10010 N. Torrey Pines Road, La Jolla, CA 92037, USA Received 5 December 2002; accepted 5 December 2002
In his review “Behavioral–analytical studies of the role of head movements in depth perception in insects, birds and mammals” Dr. Kral summarizes the occurrence and significance of head movements for motion parallax in a variety of animal groups ranging from insects to birds and mammals, excluding primates. He concludes that experimental evidence clearly shows that head movements and motion parallax are used for the estimation of distance in insects, birds and rodents but that there is not enough experimental data to conclusively show the role of head movements in larger mammals. He continues to discuss how the visual information gained by head movements is translated into distance information and what the adaptive significance of head movements are across the species. The term motion parallax describes the phenomenon that objects located at different distances from an observer seem to move at different speed through the visual field of the observer when the observer moves. Objects that are close to the observer move faster over the retina than objects farther away. This phenomenon allows the estimation of a depth map of the environment and thus the relative distance between objects and between objects and the observer. 夽 Open peer comment on Karl Kral: Behavioural–analytical studies of the role of head movements in depth perception in insects, birds and mammals. E-mail address: [email protected] (M. Wicklein).
Additionally, if the movement speed of the observer is known the apparent object speed can be used to calculate the real distance between the observer and the object. Motion parallax is created by any movements of the animal through its environment. These movements can include whole body movements, as when the animal is walking or flying, as well as head movements as discussed in this review. Kral concentrates in his review on a rather specific scenario, namely that of a stationary observer trying to estimate the distance to another object, in most cases this is the estimation of the distance to a prey from a location the predator is perching on. In these cases the animals use head movements to generate the necessary retinal displacements of the objects in their environment (“peering”). Head movements constitute a very striking and important way of generating motion parallax from movement but are not the only way to achieve it. For example bees have been shown to use whole body movements during flight to create motion parallax that is then used to compute depth and distance as reported by Lehrer (1998). Schuster et al. (2002) also show that walking Drosophila can use the motion parallax created by their movement for distance measurement. In all these cases the animals use controlled and measured self-generated motion to elicit motion parallax and for the visual system and subsequent processing centers in the brain it seems irrelevant whether the self motion is a movement of the whole body or just motion of the head.
0376-6357/$ – see front matter © 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0376-6357(03)00056-1
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M. Wicklein / Behavioural Processes 64 (2003) 17–19
Motion parallax is one of many different ways of estimating depth from visual clues. Some other possible mechanisms for computing depth or distance that have been identified and are used in concert with motion parallax are stereopsis, occlusion, vergence and looming (Collett, 1996; Fukushima et al., 2002; Malik et al., 1999; Sun and Frost, 1998; Wicklein and Strausfeld, 2000; Wicklein and Sejnowski, 2001). It is therefore important to try and preen these different mechanisms apart to be able to investigate each one in isolation. In insects many mechanisms for depth perception accessible for vertebrates like vergence movements of the eyes or accommodation can be excluded due to the structure of the insects visual system. The group of mechanisms can be even more constrained in the specific behavioral situation of an ambush predator like the praying mantis that sits motionless except for its head peering movements and then executes a very well defined and measurable maneuver when it strikes its prey. But even in such a behavioral paradigm it seems hard to exactly determine the underlying mechanism for depth perception. Kral and his coworkers interpret their experiments such that the peering movements are executed by the mantids to generate motion parallax which in turn is used for the measurement of distance to the prey. In contrast to that Rossel and coworkers hypothesize that the mechanism used by mantids for distance estimation is binocular stereopsis (Rossel, 1983, 1996; Rossel et al., 1992). Peering, in this interpretation, serves to increase the distance between the eyes, serving to allow stereopsis then used to measure distance. If the interpretation of the use of head motion is controversial in a behavioral situation in which the possible use of depth perception mechanisms was so limited, even more caution should be used in interpreting the data in species and situations where more mechanisms could play a role in determining depth. Kral suggests in his review that head movements as a way to generate motion parallax developed to break camouflage similarly to the argument brought forward by Julesz (1971) in connection with stereopsis. An alternative view could be that motion parallax by its nature is a by-product of movement in a structured environment and used by animals as one of the mechanisms to create a depth map of the environment. The
determination of the 3-D structure and the relative position of objects in respect to each other and even more so in respect to the animal is crucial for any moving animal, because animals have to know the distance to objects to avoid collisions and maintain safe or stable distances from objects, etc. in order to maneuver through a structured environment. On the other hand, head movements are executed by many animals out of a variety of different reasons, to fixate a moving object, to keep the visual world stable while moving, etc. and are in most cases well controlled and monitored by the animal. These head movements will generate motion parallax as a by-product. Consequently the neuronal circuits to analyze motion parallax should be available in all animals able to move fast through a structured environment, and in many animals head movements or body movements are already used for other purposes. Thus, it can be hypothesized that some animals (including owls and mantids) simply ritualized the already existing head movements into very well defined peering movements and utilized the already existing neuronal networks for analyzing motion parallax in the behavioral context of localizing prey while remaining stationary.
References Collett, T.S., 1996. Vision: simple stereopsis. Curr. Biol. 6 (11), 1392–1395. Fukushima, K., Yamanobe, T., Shinmei, Y., Fukushima, J., Kurkin, S., Peterson, B.W., 2002. Coding of smooth eye movements in three-dimensional space by frontal cortex. Nature 12 (419), 157–162. Julesz, B., 1971. Foundations of Cyclopean Perception. University of Chicago Press, Chicago 11. Lehrer, M., 1998. Looking all around: honeybees use different cues in different eye regions. J. Exp. Biol. 201, 3275–3292. Malik, J., Anderson, B.L., Charowhas, C.E., 1999. Stereoscopic occlusion junctions. Nat. Neurosci. 2 (9), 840–843. Schuster, S., Strauss, R., Goetz, K.G., 2002. Virtual-reality techniques resolve the visual cues used by fruit flies to evaluate object distance. Curr. Biol. 17 (12), 1591–1594. Sun, H., Frost, B.J., 1998. Computation of different optical variables of looming objects in pigeon nucleus rotundus neurons. Nat. Neurosci. 1 (4), 161–163. Rossel, S., 1983. Binocular stereopsis in an insect. Nature 302, 821–822. Rossel, S., 1996. Binocular vision in insects: how mantids solve the correspondence problem. Proc. Natl. Acad. Sci. USA 93, 13229–13232.
M. Wicklein / Behavioural Processes 64 (2003) 17–19 Rossel, S., Mathis, U., Collett, T., 1992. Vertical disparity and binocular vision in the praying mantis. Vis. Neurosci. 8 (2), 165–170. Wicklein, M., Sejnowski, T.J., 2001. Perception of change in depth in the hummingbird hawkmoth Manduca sexta (Sphingidae,
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Lepidoptera): comparing a model and looming neurons. Neurocomputing 38 (40), 1595–1602. Wicklein, M., Strausfeld, N.J., 2000. Organization and significance of neurons that detect change of visual depth in the hawk moth Manduca sexta. J. Comp. Neurol. 424 (2), 356–376.
Mini-review
Head movements and depth perception夽 Martina Wicklein Computational Neurobiology Laboratory, Howard Hughes Medical Institute, Salk Institute, 10010 N. Torrey Pines Road, La Jolla, CA 92037, USA Received 5 December 2002; accepted 5 December 2002
In his review “Behavioral–analytical studies of the role of head movements in depth perception in insects, birds and mammals” Dr. Kral summarizes the occurrence and significance of head movements for motion parallax in a variety of animal groups ranging from insects to birds and mammals, excluding primates. He concludes that experimental evidence clearly shows that head movements and motion parallax are used for the estimation of distance in insects, birds and rodents but that there is not enough experimental data to conclusively show the role of head movements in larger mammals. He continues to discuss how the visual information gained by head movements is translated into distance information and what the adaptive significance of head movements are across the species. The term motion parallax describes the phenomenon that objects located at different distances from an observer seem to move at different speed through the visual field of the observer when the observer moves. Objects that are close to the observer move faster over the retina than objects farther away. This phenomenon allows the estimation of a depth map of the environment and thus the relative distance between objects and between objects and the observer. 夽 Open peer comment on Karl Kral: Behavioural–analytical studies of the role of head movements in depth perception in insects, birds and mammals. E-mail address: [email protected] (M. Wicklein).
Additionally, if the movement speed of the observer is known the apparent object speed can be used to calculate the real distance between the observer and the object. Motion parallax is created by any movements of the animal through its environment. These movements can include whole body movements, as when the animal is walking or flying, as well as head movements as discussed in this review. Kral concentrates in his review on a rather specific scenario, namely that of a stationary observer trying to estimate the distance to another object, in most cases this is the estimation of the distance to a prey from a location the predator is perching on. In these cases the animals use head movements to generate the necessary retinal displacements of the objects in their environment (“peering”). Head movements constitute a very striking and important way of generating motion parallax from movement but are not the only way to achieve it. For example bees have been shown to use whole body movements during flight to create motion parallax that is then used to compute depth and distance as reported by Lehrer (1998). Schuster et al. (2002) also show that walking Drosophila can use the motion parallax created by their movement for distance measurement. In all these cases the animals use controlled and measured self-generated motion to elicit motion parallax and for the visual system and subsequent processing centers in the brain it seems irrelevant whether the self motion is a movement of the whole body or just motion of the head.
0376-6357/$ – see front matter © 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0376-6357(03)00056-1
18
M. Wicklein / Behavioural Processes 64 (2003) 17–19
Motion parallax is one of many different ways of estimating depth from visual clues. Some other possible mechanisms for computing depth or distance that have been identified and are used in concert with motion parallax are stereopsis, occlusion, vergence and looming (Collett, 1996; Fukushima et al., 2002; Malik et al., 1999; Sun and Frost, 1998; Wicklein and Strausfeld, 2000; Wicklein and Sejnowski, 2001). It is therefore important to try and preen these different mechanisms apart to be able to investigate each one in isolation. In insects many mechanisms for depth perception accessible for vertebrates like vergence movements of the eyes or accommodation can be excluded due to the structure of the insects visual system. The group of mechanisms can be even more constrained in the specific behavioral situation of an ambush predator like the praying mantis that sits motionless except for its head peering movements and then executes a very well defined and measurable maneuver when it strikes its prey. But even in such a behavioral paradigm it seems hard to exactly determine the underlying mechanism for depth perception. Kral and his coworkers interpret their experiments such that the peering movements are executed by the mantids to generate motion parallax which in turn is used for the measurement of distance to the prey. In contrast to that Rossel and coworkers hypothesize that the mechanism used by mantids for distance estimation is binocular stereopsis (Rossel, 1983, 1996; Rossel et al., 1992). Peering, in this interpretation, serves to increase the distance between the eyes, serving to allow stereopsis then used to measure distance. If the interpretation of the use of head motion is controversial in a behavioral situation in which the possible use of depth perception mechanisms was so limited, even more caution should be used in interpreting the data in species and situations where more mechanisms could play a role in determining depth. Kral suggests in his review that head movements as a way to generate motion parallax developed to break camouflage similarly to the argument brought forward by Julesz (1971) in connection with stereopsis. An alternative view could be that motion parallax by its nature is a by-product of movement in a structured environment and used by animals as one of the mechanisms to create a depth map of the environment. The
determination of the 3-D structure and the relative position of objects in respect to each other and even more so in respect to the animal is crucial for any moving animal, because animals have to know the distance to objects to avoid collisions and maintain safe or stable distances from objects, etc. in order to maneuver through a structured environment. On the other hand, head movements are executed by many animals out of a variety of different reasons, to fixate a moving object, to keep the visual world stable while moving, etc. and are in most cases well controlled and monitored by the animal. These head movements will generate motion parallax as a by-product. Consequently the neuronal circuits to analyze motion parallax should be available in all animals able to move fast through a structured environment, and in many animals head movements or body movements are already used for other purposes. Thus, it can be hypothesized that some animals (including owls and mantids) simply ritualized the already existing head movements into very well defined peering movements and utilized the already existing neuronal networks for analyzing motion parallax in the behavioral context of localizing prey while remaining stationary.
References Collett, T.S., 1996. Vision: simple stereopsis. Curr. Biol. 6 (11), 1392–1395. Fukushima, K., Yamanobe, T., Shinmei, Y., Fukushima, J., Kurkin, S., Peterson, B.W., 2002. Coding of smooth eye movements in three-dimensional space by frontal cortex. Nature 12 (419), 157–162. Julesz, B., 1971. Foundations of Cyclopean Perception. University of Chicago Press, Chicago 11. Lehrer, M., 1998. Looking all around: honeybees use different cues in different eye regions. J. Exp. Biol. 201, 3275–3292. Malik, J., Anderson, B.L., Charowhas, C.E., 1999. Stereoscopic occlusion junctions. Nat. Neurosci. 2 (9), 840–843. Schuster, S., Strauss, R., Goetz, K.G., 2002. Virtual-reality techniques resolve the visual cues used by fruit flies to evaluate object distance. Curr. Biol. 17 (12), 1591–1594. Sun, H., Frost, B.J., 1998. Computation of different optical variables of looming objects in pigeon nucleus rotundus neurons. Nat. Neurosci. 1 (4), 161–163. Rossel, S., 1983. Binocular stereopsis in an insect. Nature 302, 821–822. Rossel, S., 1996. Binocular vision in insects: how mantids solve the correspondence problem. Proc. Natl. Acad. Sci. USA 93, 13229–13232.
M. Wicklein / Behavioural Processes 64 (2003) 17–19 Rossel, S., Mathis, U., Collett, T., 1992. Vertical disparity and binocular vision in the praying mantis. Vis. Neurosci. 8 (2), 165–170. Wicklein, M., Sejnowski, T.J., 2001. Perception of change in depth in the hummingbird hawkmoth Manduca sexta (Sphingidae,
19
Lepidoptera): comparing a model and looming neurons. Neurocomputing 38 (40), 1595–1602. Wicklein, M., Strausfeld, N.J., 2000. Organization and significance of neurons that detect change of visual depth in the hawk moth Manduca sexta. J. Comp. Neurol. 424 (2), 356–376.