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Binocular depth perception in the meerkat (Suricata suricatta)
0042-6989/83 $3.00+ 0.00 Copyright 0 1983Pergamon Press Ltd
VisionRes. Vol. 23, NO. 10, pp. 965-969, 1983 Printed in Great Britain. All rights reserved
BINOCULAR
DEPTH
PERCEPTION
(SURICATA
IN THE MEERKAT
SURICATTA)
G. MORAN, B. TIMNEY,* L. SORENSENand B. DE~ROCHERS Department of Psychology, University of Western Ontario, London, Ontario, Canada N6A 5C2 (Received 20 December 1982; in revised form 24 February 1983) Abstract-Although it has been widely assumed that mammals with frontally placed eyes have stereoscopic vision, there is actually a paucity of supporting evidence. We have measured monocular and binocular depth perception in the meerkat (Suricata suricattu), obtaining strong evidence for the presence of stereopsis. The data provide additional evidence for the generality of stereoscopic vision across many different species. Meerkat
Visual acuity
Stereopsis
The presence of laterally separated, frontal eyes with overlapping visual fields provides the basis for stereopsis, which is the ability to use retinal disparity as a cue for making fine depth discriminations. Although several authors have argued that stereopsis is a product of mammalian evolution, reaching its culmination among the primates, (Collins, 1922; Le Gros Clark, 1959; Walls, 1942) there is actually very little empirical evidence for its existence in mammals. In fact, there has been more emphasis upon nonmammalian species than mammals themselves. Stereoscopic vision has been described in toads (Collett, 1977), falcons (Fox et al., 1977) and pigeons (McFadden and Wild, 1982) and there are indications of its presence in owls (Pettigrew and Konishi, 1976). There is even suggestive evidence for the use of disparity cues by jumping spiders (Forster, 1979). Among non-human mammals, however, stereopsis has been demonstrated only in the cat (Fox and Blake, 1971) and rhesus monkey (Bough, 1970). The present study was undertaken to provide additional evidence for the use of retinal disparity cues in mammals. We measured binocular and monocular depth thresholds in the meerkat (Suricata suricatta) and obtained good evidence that the meerkat possesses stereopsis. Meerkats are diurnal social carnivores and members of the mongoose family, Herpestinue, (see Fig. 1). They are found in arid regions of southern Africa and appear to be highly visual animals (Ewer, 1963; Lynch, 1980). Their diet consists almost entirely of insects which they seek out under rocks and in rotting tree stumps. Although both tactile and olfactory cues must be used, it seems likely that their foraging would be greatly assisted by a high level of visual acuity and accurate spatial vision. We have observed also in our studies of captive animals,
*To whom correspondence
should
be addressed. 965
(unpublished observations), that one member of the colony acts as a “sentinel” at almost all times, providing warning calls at the appearance of potential predators, even at great distances. We tested a tame, adult male which had been rejected from the colony at Toronto Metropolitan Zoo and subsequently hand-reared. All thresholds were obtained using the jumping stand technique developed by Mitchell et al. (1977; 1979). The animal adapted well to this method of testing and jumped confidently from heights of up to 70 cm. In order to establish that any limitations in depth perception were not due to poor visual acuity, that ability was measured first. The general procedure was similar for both acuity and depth perception measures. Briefly, the meerkat was trained to jump from a raised platform onto one of two adjacent landing surfaces. One of these contained the positive stimulus. A correct jump was rewarded with a small amount of beef baby food. An error was signalled by a loud, high frequency tone (95 dB, 4500 Hz). For acuity measurements the animal was required to discriminate between a high-contrast, square wave grating and a gray card of equivalent space-averaged luminance (Mitchell et al., 1977). After initial training, a preliminary threshold estimate was obtained using a psychophysical staircase procedure. Final testing was completed using the method of constant in which different stripe widths were stimuli, presented randomly in blocks of five trials. Testing was repeated daily until a minimum of 30 trials had been run at each spatial frequency. Depth thresholds were obtained in a similar fashion except that the discrimination was between the closer and more distant of two random arrays of dots, the separation of which could be varied in small steps. Testing was carried out binocularly and also monocularly, when an opaque occluder was placed over one eye.
966
G.
MORAN
The data are presented in the form of “frequency of seeing” functions. For acuity, percentage correct has been plotted as a function of spatial frequency in Fig. 2(A). Threshold has been interpolated as the point at which the function crosses the 70% correct line. It may be seen that for low spatial frequencies performance is very good, but declines systematically thereafter. The threshold estimate is 6.3 c/deg. The assumption underlying the depth discrimination measure is that any superiority of binocular performance over monocular results from the use of uniquely binocular depth cues, of which the most important is retinal disparity (Mitchell rt al., 1979). For this reason, depth discrimination performance is plotted as a function of retinal disparity. Obviously, this has no functional meaning in the context of monocular viewing, but for comparison purposes we have calculated the disparity which would have been present if both eyes were open. The results are shown in Fig. 2(B). Binocularly, performance was very systematic and the threshold of IO min is equivalent to a separation of about 5 cm from a viewing distance of 65cm. When the occluder was in place however, the task became impossible and performance fell to chance levels. This was not due to the presence of the occluder because when additional monocular cues were provided. discrimination improved markedly. By removing the mask covering the target surfaces (Timney, 1981) and allowing the animal to view the internal mechanisms of the apparatus. such cues as interposition and a perspective view became available. The position of the higher side was very obvious when the mask was not in place. Under normal testing conditions there are a number of monocular cues which are potentially available in the apparatus we used, including relative dot density, relative size differences between the dots and motion parallax. At threshold for the meerkat the relative size difference amounts to about 81;,, a difference which was not obvious to human observers viewing from the position of the jumping stand. In Fact. in the absence of head movements, even large separations are barely discriminable monocularly. Motion parallax is potentially a much more powerful cue (Rogers and Graham, 1982). but we have found in our own work with both cats and humans there is a large amount of individual variability with respect to monocular thresholds. While it is possible that our subject was assisted by motion parallax cues, or indeed any other monocular cue, the superiority of the binocular threshold indicates that the binocular cues were more powerful.* *Although these data suggest very strongly that the meera definitive answer may be kat possesses stereopsis, obtained only through the use of “pure disparity” stimuli, such as random-dot stereograms (Julesz, 1971). Unfortunately. such tests typically require the wearing of goggles which many animais. including meerkats, do not tolerate willingly. For this reason we chose to gather our Initial data usmg the simpler procedure.
PI ul.
100
r
Spatial frequency (c/deg) 100
r \ ..* I
z
70
/__---_-____---_____--------_-\__
50
I
I
too
I 80
I 60
I 40
I 20
1
0
Retinal disparity fmin/arc) Fig. 2. (A) Visual resolution in the meerkat. Percentage of correct choices is plotted as a function of the spatial frequency of a high contrast square wave grating. Testing was binocular and each data point is derived from at least 30 and usually 50 trials. (B) Binocular and monocular depth discrimination. Percent correct is plotted as a function of retinal disparity under binocular testing conditions (solid squares). For monocular testing (open squares) the measure is the disparity which would have been present had both eyes been open.
Data from a related species, the mongoose (Nerpesres auropunctarus) suggest that members of this family may have a duplex retina (Hope er al., 1982), but nothing is known specifically about the organisation of the visual pathways in the meerkat. It is evident, however, that the animal has sophisticated visual skills, well matched to its ecology. The strong presumptive evidence for stereopsis leads to the prediction that the meerkat, like the cat (Barlow ef al., 1976) and the monkey (Poggio and Fischer, t977), should possess disparity tuned neurones in the visual cortex. Such a finding would provide additional support for the view that these neurones are the underlying mechanisms of stereoscopic vision. Further, the suitability of the meerkat for behavioural testing may make this animal a useful model in the study of binocular vision.
Acknowled~emenis-This research was supported by grants from the Natural Science and Engineering Research Council of Canada to G.M. and B.T. We thank John Orphan for constructing the apparatus.
Fig. I. Meerkat (Suricatn s~ricacta). Note the frontal eyes with extensive binocular overlap.
967
Depth
perception
REFERENCES Barlow H. B., Blakemore C. and Pettigrew J. D. (1967) The neural mechanism of binocular depth discrimination. J. Physiol. 193, 327-343. Bough E. W. (1970) Stereoscopic vision in the macaque monkey: a behavioural demonstration. Nature 225, 42-44. Collett T. (1977) Stereopsis in toads. Nature 267, 349-351. Collins E. T. (1922) Ahoreal Life and the Evolution of the Humun Eye. Lea & Feninger, Philadelphia. Ewer R. F. (1963) The behavior of the meerkat, Suricata .suricatta (Schreber). Z. Tierpsychol. 20, 570-607. Forster L. M. (1979)Visual mechanisms of hunting behaviour in Trife planiceps, a jumping spider (Araneae: Salticidae). Ne+r Zealand J. Zool. 6, 79-93. Fox R. and Blake R. R. (1971) Stereoscopic vision in the cat. Nuture 253, 55-56. Fox R., Lehmkuhle S. W. and Bush R. C. (1971) Stereopsis in the falcon. Science 197, 79-81. Hope G. M., Dawson W. W., Parmer R.. Hawthorne M. N. and Nellis D. M. (1982) The mongoose: a potentially useful eye for retina research. Invest. Ophthal. visual Sci., Suppl. 22, 56. Julesz B. (1971) Foundations of Cyclopean Perception. Univ. of Chicago Press, Chicago. Le Gros Clark W. E. (1959) The Antecedents of Man. Quadrangle Books, Chicago.
in the meerkat
969
Lynch C. D. (1980) Ecology of the suricate, Suricata suricatta and yellow mongoose, Cynictis penicillata with special reference to their reproduction. Mem. Nasionale Museum 14, l-145. McFadden S. and Wild J. M. (1982) Stereopsis as a primary cue for depth perception in the pigeon. Sot. Neurosci. Absir. 8, 942. Mitchell D. E., Giffin F. and Timney B. (1977) A behavioural technique for the rapid assessment of the visual capabilities of kittens. Perception 6, 18I-193. Mitchell D. E., Kaye M. and Timney B. (1979) Assessment of depth perception in cats. Perception 8, 389-396. Pettigrew J. D. and Konishi M. (1976) Neurons selective for o&ttation and binocular disparity in the visual Wulst of the barn owl (Tvfo alba). Science 193, 675-678. Poggio G. F. and Fischer B. (1977) Binocular interaction and depth sensitivity in striate and prestriate cortex of behaving rhesus monkey. J. Neurophysiol. 40, 139221405. Rogers B. J. and Graham M. (1982) Similarities between motion parallax and stereopsis in human depth perception. Visual Res. 22, 261-270. Timney B. (1981) Development of binocular depth perception in kittens. Invest. Ophthal. visuul Sci. 21, 493-496. Walls G. L. (1942) The Vertebrate Eye and its Adaptive Radiation. The Cranbrook Press, Bloomfield Hills. MI.
VisionRes. Vol. 23, NO. 10, pp. 965-969, 1983 Printed in Great Britain. All rights reserved
BINOCULAR
DEPTH
PERCEPTION
(SURICATA
IN THE MEERKAT
SURICATTA)
G. MORAN, B. TIMNEY,* L. SORENSENand B. DE~ROCHERS Department of Psychology, University of Western Ontario, London, Ontario, Canada N6A 5C2 (Received 20 December 1982; in revised form 24 February 1983) Abstract-Although it has been widely assumed that mammals with frontally placed eyes have stereoscopic vision, there is actually a paucity of supporting evidence. We have measured monocular and binocular depth perception in the meerkat (Suricata suricattu), obtaining strong evidence for the presence of stereopsis. The data provide additional evidence for the generality of stereoscopic vision across many different species. Meerkat
Visual acuity
Stereopsis
The presence of laterally separated, frontal eyes with overlapping visual fields provides the basis for stereopsis, which is the ability to use retinal disparity as a cue for making fine depth discriminations. Although several authors have argued that stereopsis is a product of mammalian evolution, reaching its culmination among the primates, (Collins, 1922; Le Gros Clark, 1959; Walls, 1942) there is actually very little empirical evidence for its existence in mammals. In fact, there has been more emphasis upon nonmammalian species than mammals themselves. Stereoscopic vision has been described in toads (Collett, 1977), falcons (Fox et al., 1977) and pigeons (McFadden and Wild, 1982) and there are indications of its presence in owls (Pettigrew and Konishi, 1976). There is even suggestive evidence for the use of disparity cues by jumping spiders (Forster, 1979). Among non-human mammals, however, stereopsis has been demonstrated only in the cat (Fox and Blake, 1971) and rhesus monkey (Bough, 1970). The present study was undertaken to provide additional evidence for the use of retinal disparity cues in mammals. We measured binocular and monocular depth thresholds in the meerkat (Suricata suricatta) and obtained good evidence that the meerkat possesses stereopsis. Meerkats are diurnal social carnivores and members of the mongoose family, Herpestinue, (see Fig. 1). They are found in arid regions of southern Africa and appear to be highly visual animals (Ewer, 1963; Lynch, 1980). Their diet consists almost entirely of insects which they seek out under rocks and in rotting tree stumps. Although both tactile and olfactory cues must be used, it seems likely that their foraging would be greatly assisted by a high level of visual acuity and accurate spatial vision. We have observed also in our studies of captive animals,
*To whom correspondence
should
be addressed. 965
(unpublished observations), that one member of the colony acts as a “sentinel” at almost all times, providing warning calls at the appearance of potential predators, even at great distances. We tested a tame, adult male which had been rejected from the colony at Toronto Metropolitan Zoo and subsequently hand-reared. All thresholds were obtained using the jumping stand technique developed by Mitchell et al. (1977; 1979). The animal adapted well to this method of testing and jumped confidently from heights of up to 70 cm. In order to establish that any limitations in depth perception were not due to poor visual acuity, that ability was measured first. The general procedure was similar for both acuity and depth perception measures. Briefly, the meerkat was trained to jump from a raised platform onto one of two adjacent landing surfaces. One of these contained the positive stimulus. A correct jump was rewarded with a small amount of beef baby food. An error was signalled by a loud, high frequency tone (95 dB, 4500 Hz). For acuity measurements the animal was required to discriminate between a high-contrast, square wave grating and a gray card of equivalent space-averaged luminance (Mitchell et al., 1977). After initial training, a preliminary threshold estimate was obtained using a psychophysical staircase procedure. Final testing was completed using the method of constant in which different stripe widths were stimuli, presented randomly in blocks of five trials. Testing was repeated daily until a minimum of 30 trials had been run at each spatial frequency. Depth thresholds were obtained in a similar fashion except that the discrimination was between the closer and more distant of two random arrays of dots, the separation of which could be varied in small steps. Testing was carried out binocularly and also monocularly, when an opaque occluder was placed over one eye.
966
G.
MORAN
The data are presented in the form of “frequency of seeing” functions. For acuity, percentage correct has been plotted as a function of spatial frequency in Fig. 2(A). Threshold has been interpolated as the point at which the function crosses the 70% correct line. It may be seen that for low spatial frequencies performance is very good, but declines systematically thereafter. The threshold estimate is 6.3 c/deg. The assumption underlying the depth discrimination measure is that any superiority of binocular performance over monocular results from the use of uniquely binocular depth cues, of which the most important is retinal disparity (Mitchell rt al., 1979). For this reason, depth discrimination performance is plotted as a function of retinal disparity. Obviously, this has no functional meaning in the context of monocular viewing, but for comparison purposes we have calculated the disparity which would have been present if both eyes were open. The results are shown in Fig. 2(B). Binocularly, performance was very systematic and the threshold of IO min is equivalent to a separation of about 5 cm from a viewing distance of 65cm. When the occluder was in place however, the task became impossible and performance fell to chance levels. This was not due to the presence of the occluder because when additional monocular cues were provided. discrimination improved markedly. By removing the mask covering the target surfaces (Timney, 1981) and allowing the animal to view the internal mechanisms of the apparatus. such cues as interposition and a perspective view became available. The position of the higher side was very obvious when the mask was not in place. Under normal testing conditions there are a number of monocular cues which are potentially available in the apparatus we used, including relative dot density, relative size differences between the dots and motion parallax. At threshold for the meerkat the relative size difference amounts to about 81;,, a difference which was not obvious to human observers viewing from the position of the jumping stand. In Fact. in the absence of head movements, even large separations are barely discriminable monocularly. Motion parallax is potentially a much more powerful cue (Rogers and Graham, 1982). but we have found in our own work with both cats and humans there is a large amount of individual variability with respect to monocular thresholds. While it is possible that our subject was assisted by motion parallax cues, or indeed any other monocular cue, the superiority of the binocular threshold indicates that the binocular cues were more powerful.* *Although these data suggest very strongly that the meera definitive answer may be kat possesses stereopsis, obtained only through the use of “pure disparity” stimuli, such as random-dot stereograms (Julesz, 1971). Unfortunately. such tests typically require the wearing of goggles which many animais. including meerkats, do not tolerate willingly. For this reason we chose to gather our Initial data usmg the simpler procedure.
PI ul.
100
r
Spatial frequency (c/deg) 100
r \ ..* I
z
70
/__---_-____---_____--------_-\__
50
I
I
too
I 80
I 60
I 40
I 20
1
0
Retinal disparity fmin/arc) Fig. 2. (A) Visual resolution in the meerkat. Percentage of correct choices is plotted as a function of the spatial frequency of a high contrast square wave grating. Testing was binocular and each data point is derived from at least 30 and usually 50 trials. (B) Binocular and monocular depth discrimination. Percent correct is plotted as a function of retinal disparity under binocular testing conditions (solid squares). For monocular testing (open squares) the measure is the disparity which would have been present had both eyes been open.
Data from a related species, the mongoose (Nerpesres auropunctarus) suggest that members of this family may have a duplex retina (Hope er al., 1982), but nothing is known specifically about the organisation of the visual pathways in the meerkat. It is evident, however, that the animal has sophisticated visual skills, well matched to its ecology. The strong presumptive evidence for stereopsis leads to the prediction that the meerkat, like the cat (Barlow ef al., 1976) and the monkey (Poggio and Fischer, t977), should possess disparity tuned neurones in the visual cortex. Such a finding would provide additional support for the view that these neurones are the underlying mechanisms of stereoscopic vision. Further, the suitability of the meerkat for behavioural testing may make this animal a useful model in the study of binocular vision.
Acknowled~emenis-This research was supported by grants from the Natural Science and Engineering Research Council of Canada to G.M. and B.T. We thank John Orphan for constructing the apparatus.
Fig. I. Meerkat (Suricatn s~ricacta). Note the frontal eyes with extensive binocular overlap.
967
Depth
perception
REFERENCES Barlow H. B., Blakemore C. and Pettigrew J. D. (1967) The neural mechanism of binocular depth discrimination. J. Physiol. 193, 327-343. Bough E. W. (1970) Stereoscopic vision in the macaque monkey: a behavioural demonstration. Nature 225, 42-44. Collett T. (1977) Stereopsis in toads. Nature 267, 349-351. Collins E. T. (1922) Ahoreal Life and the Evolution of the Humun Eye. Lea & Feninger, Philadelphia. Ewer R. F. (1963) The behavior of the meerkat, Suricata .suricatta (Schreber). Z. Tierpsychol. 20, 570-607. Forster L. M. (1979)Visual mechanisms of hunting behaviour in Trife planiceps, a jumping spider (Araneae: Salticidae). Ne+r Zealand J. Zool. 6, 79-93. Fox R. and Blake R. R. (1971) Stereoscopic vision in the cat. Nuture 253, 55-56. Fox R., Lehmkuhle S. W. and Bush R. C. (1971) Stereopsis in the falcon. Science 197, 79-81. Hope G. M., Dawson W. W., Parmer R.. Hawthorne M. N. and Nellis D. M. (1982) The mongoose: a potentially useful eye for retina research. Invest. Ophthal. visual Sci., Suppl. 22, 56. Julesz B. (1971) Foundations of Cyclopean Perception. Univ. of Chicago Press, Chicago. Le Gros Clark W. E. (1959) The Antecedents of Man. Quadrangle Books, Chicago.
in the meerkat
969
Lynch C. D. (1980) Ecology of the suricate, Suricata suricatta and yellow mongoose, Cynictis penicillata with special reference to their reproduction. Mem. Nasionale Museum 14, l-145. McFadden S. and Wild J. M. (1982) Stereopsis as a primary cue for depth perception in the pigeon. Sot. Neurosci. Absir. 8, 942. Mitchell D. E., Giffin F. and Timney B. (1977) A behavioural technique for the rapid assessment of the visual capabilities of kittens. Perception 6, 18I-193. Mitchell D. E., Kaye M. and Timney B. (1979) Assessment of depth perception in cats. Perception 8, 389-396. Pettigrew J. D. and Konishi M. (1976) Neurons selective for o&ttation and binocular disparity in the visual Wulst of the barn owl (Tvfo alba). Science 193, 675-678. Poggio G. F. and Fischer B. (1977) Binocular interaction and depth sensitivity in striate and prestriate cortex of behaving rhesus monkey. J. Neurophysiol. 40, 139221405. Rogers B. J. and Graham M. (1982) Similarities between motion parallax and stereopsis in human depth perception. Visual Res. 22, 261-270. Timney B. (1981) Development of binocular depth perception in kittens. Invest. Ophthal. visuul Sci. 21, 493-496. Walls G. L. (1942) The Vertebrate Eye and its Adaptive Radiation. The Cranbrook Press, Bloomfield Hills. MI.