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Adaptation and the neural code for visual form
374
Brain Research, 52 (1973) 374-377 ~ Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
Adaptation and the neural code for visual form
ROBERT P. ERICKSON
Departments of Psychology and Physiology, Duke University, Durham, N.C. 27706 (U.S.A.)
(Accepted December 5th, 1972)
A recent wealth of neurophysiologic and psychophysical data has suggested the existence of rectilinear form detectors in the human visual system 1-3. This conclusion requires as part of normal experimental design a demonstration, using the same methodology, of the relative absence of psychophysical and 'neural' processes corresponding to other visual forms. Evidence of processes for a variety of other visual forms would either weaken the logic for the rectilinear form detectors, or would make a case for many types of detectors. In either circumstance, the case for the presence or singularity of rectilinear neural processes is not complete without the 'control' cases. That adaptation does occur with other than straight lines may be easily demonstrated. A consideration of these 'control' cases in comparison with the most effective rectilinear stimuli leads to some insights about the adaptation process, and about the neural organization of form vision. In Fig. 1 are shown 3 examples of visual forms with which adaptation to nonrectilinear forms may be demonstrated. In part A of the figure, adaptation in the test figure on the right can be demonstrated following the usual conditioning procedures of inspecting the left side of the figure for about 45 sec. To avoid after-images, the point of fixation must move, for example around the circle provided in the center. The parallelograms on the right will then appear slightly fainter than the diagonal lines, indicating partial adaptation of the parallelograms. This adaptation, obtained with 5 subjects, follows the general form of adaptation shown earlier, although we have not studied it in such great detail. Adaptation in this case is expected on the grounds that parallelograms are composed of straight lines, and adaptation to straight lines has been demonstrated. But strictly following the logic of the earlier experiments, that adaptation to a particular form is evidence of the existence of neural mechanisms for that form, the existence of
Fig. t. Figures to demonstrate adaptation with other than straight-line gratings. In all 3 examples, inspection of the conditioning figure on the left will result in a brief and partial fading of the same figure on the right relative to the diagonal lines. In all 3 examples the point of gaze must move continuously to avoid after-images. In A, the point of gaze may move around the fixation circle provided. In B and C, the point of gaze must be restricted to one pair of the short horizontal bars.
A
B
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C
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D
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SHORT COMMUNICATIONS
neural mechanisms for parallelograms seems to be demonstrated. At this point, the argument that adaptation to parallelograms occurs because these are composed of straight lines seems no more valid than the argument that adaptation to straight lines occurs simply because they are components of adapted parallelograms. The point here is not that there may be parallelogram detectors, but that the realm of stimuli beyond rectilinear gratings has not been adequately perused. In part B of Fig. 1, adaptation will not occur if the point of fixation is allowed to move in both horizontal and vertical directions. However, adaptation will occur, as in part A, if the point of fixation is allowed to move only in the horizontal direction at one level, and the test figure is viewed at this same level. Probably this adaptation occurs because with only horizontal movements each point of the retina is exposed only to lines of a particular orientation - - although this orientation varies from point to point on the retina. If the eye is allowed to move both vertically and horizontally each point of the eye receives stimulation from a variety of orientations, and adaptation will not occur. This is also true with part C of the figure where adaptation is seen to occur if the point of fixation during adaptation and testing is allowed to move along one of the short horizontal fixation bars. Considering the earlier studies of rectilinear figures along with the present 3 examples, the common requirement for adaptation seems to be only that each point in the retina receives a similar stimulus in the conditioning and test situations. This requirement will be met most fully with gratings of a constant spatial frequency (dissimilar spacing of the lines of the grating would cause 'different' stimuli to fall on a given retinal point with eye movement). The main implication to be drawn from these simple demonstrations is that in order to maintain similarity between the adapting and test stimuli, and thus to produce the greatest adaptation, the most efficient stimuli to use must be linear and of a given spatial frequency. This conclusion does not touch on the issue of the sensitivities of the neurons involved in the perception of forms. In other words, the psychophysical and neural adaptation studies do not speak directly to the question of the sensitivities of the individual neurons. In apparent support of the previous adaptation studies, many neural studies have suggested that individual central visual neurons are particularly sensitive to rectilinear figures 7, and perhaps even to gratings of a given spatial frequency 4,5,9. Although sensitivities to more complex figures have been amply demonstrated 6,s, and may be more common than is presently believed, sensitivities to linear figures must have some special usefulness to the organism. A clue to the nature of this usefulness may be disclosed by consideration of the sensitivities of color-coded neurons. Small populations of neurons broadly tuned to wavelengths can serve to signal all wavelengths. Such simply tuned neurons would be brought into play by almost any visual stimulus. However, as sensitivities increased in complexity beyond this simple level they would become only decreasingly activated by visual stimuli; neurons with very complex senstivities - - e.g. to a particular human face or even a particular wavelength - - would seldom, or never, be brought into play. Thus, to the extent that the number of neurons activated by any stimulus is a critical factor, neurons with rather
SHORT COMMUNICATIONS
377
simple b r o a d sensitivities, such as to ranges o f colors and ranges o f the orientation o f straight lines, would be most efficient. Thus the similarity o f conclusions between the single neuron studies and the adaptation studies m a y be fortuitous; the only experimentally feasible way to make the conditioning and test stimuli similar with a moving direction o f gaze seems to be to use simple linear stimuli at a fixed spatial frequency. However, the similarity m a y occur because the same constraints exist in both realms which independently require neural and psychophysical sensitivities to rectilinear gratings. F o r example, if the nervous system performs a Fourier-like process, the only possible sensitivity would be to straight, or nearly straight, lines. In any case, it is not clear that studies other than direct recordings from individual visual neurons have spoken critically to the issue o f their sensitivities. W h a t has been demonstrated in this and in previous adaptation studies is only that the extent o f adaptation is a direct function o f the similarity o f the conditioning and test stimuli.
1 BLAKEMORE, C., AND CAMPBELL, F. W., Adaptation to spatial stimuli, J. Physiol. (Lond.), 200
(1968) 11-13. 2 BLAKEMORE,C., AND CAMPBELL, F. W., On the existence of neurones in the human visual system
3
4
5 6 7 8 9
selectively sensitive to the orientation and size of retinal images, J. Physiol. (Lond.), 203 (1969) 237-260. BLAKEMORE, C., AND NACHMIAS, J., The orientation specificity of two visual after-effects, J. Physiol. (Lond.), 213 (1971) 157-174. CAMPBELL, F. W., CLELAND, B. G., COOPER, G. F., AND ENROTH-CUGELL,C., The angular selectivity of visual cortical cells to moving gratings, J. Physiol. (Lond.), 198 (1968) 237-250. CAMPBELL,F. W., COOPER,G. F., ROBSON,J. G., AND SACHS,M. B., The spatial selectivity of visual ceUs of the cat and the squirrel monkey, J. Physiol. (Lond.), 204 (1969) 120-121. GRoss, C. G., ROCHA-MIRANDA, C. L., AND BENDER, D. B., Visual properties ofneurones in inferotemporal cortex of the Macaque, J. Neurophysiol., 35 (1972) 96-111. HUBEL,O. H., AND WIESEL, T. N., Receptive fields, binocular interaction and functional architecture in the cat's visual cortex, J. Physiol. (Lond.), 160 (1962) 106-154. HUBEL, D. H., AND WIESEL, Z. N., Receptive fields and functional architecture in two nonstriate visual areas (18 and 19) of the cat, J. Neurophysiol., 28 (1965) 229-289. POLLEN,D. A., TAYLOR,J. H., ANDLEE,J. R., How does the striate cortex begin the reconstruction of the visual world? Science, 173 (1971) 74-77.
Brain Research, 52 (1973) 374-377 ~ Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
Adaptation and the neural code for visual form
ROBERT P. ERICKSON
Departments of Psychology and Physiology, Duke University, Durham, N.C. 27706 (U.S.A.)
(Accepted December 5th, 1972)
A recent wealth of neurophysiologic and psychophysical data has suggested the existence of rectilinear form detectors in the human visual system 1-3. This conclusion requires as part of normal experimental design a demonstration, using the same methodology, of the relative absence of psychophysical and 'neural' processes corresponding to other visual forms. Evidence of processes for a variety of other visual forms would either weaken the logic for the rectilinear form detectors, or would make a case for many types of detectors. In either circumstance, the case for the presence or singularity of rectilinear neural processes is not complete without the 'control' cases. That adaptation does occur with other than straight lines may be easily demonstrated. A consideration of these 'control' cases in comparison with the most effective rectilinear stimuli leads to some insights about the adaptation process, and about the neural organization of form vision. In Fig. 1 are shown 3 examples of visual forms with which adaptation to nonrectilinear forms may be demonstrated. In part A of the figure, adaptation in the test figure on the right can be demonstrated following the usual conditioning procedures of inspecting the left side of the figure for about 45 sec. To avoid after-images, the point of fixation must move, for example around the circle provided in the center. The parallelograms on the right will then appear slightly fainter than the diagonal lines, indicating partial adaptation of the parallelograms. This adaptation, obtained with 5 subjects, follows the general form of adaptation shown earlier, although we have not studied it in such great detail. Adaptation in this case is expected on the grounds that parallelograms are composed of straight lines, and adaptation to straight lines has been demonstrated. But strictly following the logic of the earlier experiments, that adaptation to a particular form is evidence of the existence of neural mechanisms for that form, the existence of
Fig. t. Figures to demonstrate adaptation with other than straight-line gratings. In all 3 examples, inspection of the conditioning figure on the left will result in a brief and partial fading of the same figure on the right relative to the diagonal lines. In all 3 examples the point of gaze must move continuously to avoid after-images. In A, the point of gaze may move around the fixation circle provided. In B and C, the point of gaze must be restricted to one pair of the short horizontal bars.
A
B
F
C
L J
)
(
D
>
376
SHORT COMMUNICATIONS
neural mechanisms for parallelograms seems to be demonstrated. At this point, the argument that adaptation to parallelograms occurs because these are composed of straight lines seems no more valid than the argument that adaptation to straight lines occurs simply because they are components of adapted parallelograms. The point here is not that there may be parallelogram detectors, but that the realm of stimuli beyond rectilinear gratings has not been adequately perused. In part B of Fig. 1, adaptation will not occur if the point of fixation is allowed to move in both horizontal and vertical directions. However, adaptation will occur, as in part A, if the point of fixation is allowed to move only in the horizontal direction at one level, and the test figure is viewed at this same level. Probably this adaptation occurs because with only horizontal movements each point of the retina is exposed only to lines of a particular orientation - - although this orientation varies from point to point on the retina. If the eye is allowed to move both vertically and horizontally each point of the eye receives stimulation from a variety of orientations, and adaptation will not occur. This is also true with part C of the figure where adaptation is seen to occur if the point of fixation during adaptation and testing is allowed to move along one of the short horizontal fixation bars. Considering the earlier studies of rectilinear figures along with the present 3 examples, the common requirement for adaptation seems to be only that each point in the retina receives a similar stimulus in the conditioning and test situations. This requirement will be met most fully with gratings of a constant spatial frequency (dissimilar spacing of the lines of the grating would cause 'different' stimuli to fall on a given retinal point with eye movement). The main implication to be drawn from these simple demonstrations is that in order to maintain similarity between the adapting and test stimuli, and thus to produce the greatest adaptation, the most efficient stimuli to use must be linear and of a given spatial frequency. This conclusion does not touch on the issue of the sensitivities of the neurons involved in the perception of forms. In other words, the psychophysical and neural adaptation studies do not speak directly to the question of the sensitivities of the individual neurons. In apparent support of the previous adaptation studies, many neural studies have suggested that individual central visual neurons are particularly sensitive to rectilinear figures 7, and perhaps even to gratings of a given spatial frequency 4,5,9. Although sensitivities to more complex figures have been amply demonstrated 6,s, and may be more common than is presently believed, sensitivities to linear figures must have some special usefulness to the organism. A clue to the nature of this usefulness may be disclosed by consideration of the sensitivities of color-coded neurons. Small populations of neurons broadly tuned to wavelengths can serve to signal all wavelengths. Such simply tuned neurons would be brought into play by almost any visual stimulus. However, as sensitivities increased in complexity beyond this simple level they would become only decreasingly activated by visual stimuli; neurons with very complex senstivities - - e.g. to a particular human face or even a particular wavelength - - would seldom, or never, be brought into play. Thus, to the extent that the number of neurons activated by any stimulus is a critical factor, neurons with rather
SHORT COMMUNICATIONS
377
simple b r o a d sensitivities, such as to ranges o f colors and ranges o f the orientation o f straight lines, would be most efficient. Thus the similarity o f conclusions between the single neuron studies and the adaptation studies m a y be fortuitous; the only experimentally feasible way to make the conditioning and test stimuli similar with a moving direction o f gaze seems to be to use simple linear stimuli at a fixed spatial frequency. However, the similarity m a y occur because the same constraints exist in both realms which independently require neural and psychophysical sensitivities to rectilinear gratings. F o r example, if the nervous system performs a Fourier-like process, the only possible sensitivity would be to straight, or nearly straight, lines. In any case, it is not clear that studies other than direct recordings from individual visual neurons have spoken critically to the issue o f their sensitivities. W h a t has been demonstrated in this and in previous adaptation studies is only that the extent o f adaptation is a direct function o f the similarity o f the conditioning and test stimuli.
1 BLAKEMORE, C., AND CAMPBELL, F. W., Adaptation to spatial stimuli, J. Physiol. (Lond.), 200
(1968) 11-13. 2 BLAKEMORE,C., AND CAMPBELL, F. W., On the existence of neurones in the human visual system
3
4
5 6 7 8 9
selectively sensitive to the orientation and size of retinal images, J. Physiol. (Lond.), 203 (1969) 237-260. BLAKEMORE, C., AND NACHMIAS, J., The orientation specificity of two visual after-effects, J. Physiol. (Lond.), 213 (1971) 157-174. CAMPBELL, F. W., CLELAND, B. G., COOPER, G. F., AND ENROTH-CUGELL,C., The angular selectivity of visual cortical cells to moving gratings, J. Physiol. (Lond.), 198 (1968) 237-250. CAMPBELL,F. W., COOPER,G. F., ROBSON,J. G., AND SACHS,M. B., The spatial selectivity of visual ceUs of the cat and the squirrel monkey, J. Physiol. (Lond.), 204 (1969) 120-121. GRoss, C. G., ROCHA-MIRANDA, C. L., AND BENDER, D. B., Visual properties ofneurones in inferotemporal cortex of the Macaque, J. Neurophysiol., 35 (1972) 96-111. HUBEL,O. H., AND WIESEL, T. N., Receptive fields, binocular interaction and functional architecture in the cat's visual cortex, J. Physiol. (Lond.), 160 (1962) 106-154. HUBEL, D. H., AND WIESEL, Z. N., Receptive fields and functional architecture in two nonstriate visual areas (18 and 19) of the cat, J. Neurophysiol., 28 (1965) 229-289. POLLEN,D. A., TAYLOR,J. H., ANDLEE,J. R., How does the striate cortex begin the reconstruction of the visual world? Science, 173 (1971) 74-77.