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Tilt-constant receptive fields in the kitten visual cortex
344
Brain Research, 163 (1979) 344-348 ~/Elsevier/North-Holland Biomedical Press
Tilt-constant receptive fields in the kitten visual cortex
JACQUELINE METZLER and D. NICO SPINELLI Department of Surgery, Section of Neurological Surgery, Yale University School of Medicine, New Haven, Conn. 06510 and Departments of Computer and Information Science and Psychology, University of Massachusetts, Amherst, Mass. 01003 (U.S.A.)
(Accepted November 9th, 1978)
Our perception of the visual world remains relatively constant during head or body tilt. Several recent reports4,7, 8,16 have suggested that, at least in the cat, this phenomenon of orientation or tilt-constancy might be explained by changes in the orientation specificity of about 5 ~ of the neurons in the visual cortex during head or body rotation. Units whose visual responses are modified by body tilt have also been found in the superior colliculusL Apparently, these cells all have dynamic visual properties. This report provides additional evidence that body tilt modifies the orientation specificity of certain neurons in the primary visual cortex. In an effort to examine the effects of early visual experience on the development of tilt-constant receptive fields, kittens were placed in a completely dark room from birth until 12-20 weeks of age. Beginning at 3.5 weeks of age, the kittens received daily selective visual stimulation. Each animal's total visual experience consisted of viewing a white field containing two black vertical bars with one eye while simultaneously viewing a white field with two black horizontal bars with other eye. The black bars were 1° wide and 13° long, with the center points 6 ° apart. The stimuli were mounted in goggles which the kittens wore for 4 h daily. The bars viewed by one eye were gravity-stabilized (i.e., they were free to rotate in the goggles) so that their orientation remained constant whenever the kitten tilted its head. The orthogonally oriented bars presented to the other eye were fixed in the goggles so that they maintained a constant orientation on the retina. In this way, each kitten served as its own control and the two effects could be conveniently compared. The stimuli were positioned in the goggles at the focal plane of a lens so that small changes in the position of the goggles would not affect the sharpness of focus. The eyepieces of the goggles provided a 50-60 ° field of view for each eye. Clear diffusing plastic near the ends of each eyepiece provided uniform illumination of the stimuli. The goggles were put on and removed inside the darkroom to insure that the animals received only the specified visual stimulation. The kittens quickly became accustomed to the goggles and behaved normally throughout the exposure periods. Records were taken from single units in area 17 when the kittens were between 12 and 20 weeks old. The preparation, recording and mapping techniques have been
345 described in detail in an earlier report lz. In brief, thiopental sodium (Pentothal) was injected intravenously to obtain surgical anesthesia. The kitten was placed in a stereotaxic apparatus and a small opening was made in the skin, bone and dura above the visual cortex of both hemispheres. All pressure points and incisions were infiltrated with a long-acting local anesthetic (Zyljectin). General anesthesia was then discontinued and the animal was immobilized with a continuous infusion of gallamine triethiodide (Flaxedil) (4.0 mg/kg/h) and artificially respired with a mixture of 70 N20-30 ~ 02 throughout the recording session. Core temperature was maintained at 37 ~ 1 °C. The kitten was placed 57 cm from a white tangent screen; at this distance 1 cm on the screen is equal to 1° visual angle. Contact lenses were used to correct for accommodation and protect the cornea of the eye. The optic discs were projected onto the screen with a reversible ophthalmoscope and the position of the area centralis inferred is. Electrode penetrations were made in area 17 between stereotaxic coordinates anterior-posterior --1.0 to + 1.0 mm and medial-lateral 0.5 to 1.5 mm. In the adult cat this corresponds to the region receiving projections from the area corresponds to the region receiving projections from the area centralis 14. Single-unit activity was recorded with tungsten microelectrodes. The receptive field of a cell was mapped with a black spot (1-4 ° in diameter) that was moved across a 25 ° by 25 ° white field by a computer-controlled x-y plotter. Unit activity was recorded at each of 2500 points within this field and presented on an oscilloscope screen as an integral contour display (see Fig. 1), thus displaying both the shape and the orientation of the receptive field. The general response characteristics, orientation selectivity and preferred direction of movement of each unit were also determined by manually moving light and dark bars, edges and spots across the visual field9. The receptive field of a cell was mapped when the kitten was in the standard (horizontal) position, when tilted 23 ° clockwise or counterclockwise, and again in the standard position. The shapes of the receptive fields of 94 units from the 8 kittens have been classified as either diffuse or elongated. Diffuse receptive fields have no clearly defined boundaries, with the units responding to stimulation over a large area of the visual field. Fifty-two units were of this type. One unit had a disc-shaped receptive field. The receptive fields of the remaining 41 units were classified as elongated. These units differed from those found in the normal cat in several respects: (1) they responded to input from only one eye. Normally, only 10-20 ~ of the cells in the visual cortex of the cat are monocularly activatedL As was anticipated, discordant stimulation of the two eyes resulted in a sharp reduction in binocularly driven units10; (2) when mapped with the kitten in the standard position, these units had receptive field orientations coincident with the bar pattern to which the eye had been exposed during rearing (see Fig. 1). In the normal cat, receptive fields of all orientations can be activated by both eyesg; (3) many of the elongated receptive fields were considerably larger than those of units receiving projections from the area centralis in normal cats 9. These results, however, are consistent with previously reported findings~,6,17. Barring any corrective factors, one would expect that when the immobilized animal is rotated about its longitudinal axis, the orientation of the receptive fields would rotate by the same amount and in the same direction, provided, of course, that
346
LE @
RE
J J
STANDARD ORIENTATION
TILTED CLOCKWISE 23 *
STANDARD ORIENTATION
Fig. 1. Integral contour displays of the receptive fields of two cells, each activated by a different eye. These cells were recorded from a kitten whose left eye had been exposed to two horizontal bars having a fixed retinal orientation and whose right eye had viewed two gravity-stabilized horizontal bars during development. The arrows designate the direction of stimulus movement during mapping.
one ensures that the eye remains stationary in the orbit. (The eyes were checked repeatedly throughout the experiment and caution was taken to eliminate eye movements with intravenous infusion of gallamine triethiodide and D-tubocurarine.) In this situation, the relationship between the head axis and the receptive field axis should remain constant. This is essentially what was observed for the receptive fields of those units that could be activated only by the eye that had viewed the pattern having a fixed retinal orientation during development. Upon returning the animal to the standard position, the fixed axis also returned to its original orientation. In other words, these receptive fields were not tilt-constant (Fig. 1). Twenty-two units were of this type. In contrast, the receptive field orientation of cells that could be activated only by the eye that had been exposed to the gravity-stabilized pattern during rearing
347 remained unchanged following body tilt, i.e., these cells appeared to demonstrate tiltconstancy. Nineteen units were of this classification. Integral contour displays of the receptive fields of two units - - one driven by the left eye and the other by the right eye - - are shown in Fig. 1. These units were recorded from a kitten exposed to two horizontal bars having a fixed retinal orientation with the left eye and two gravity-stabilized vertical bars with the right eye. The receptive fields of both cells were mapped when the kitten was in the standard position, when tilted 23° clockwise, and again in the standard position. Note that the two-bar receptive field - mimicking the stimulus pattern viewed during rearing - - was not tilt-constant, while the orientation of the vertically elongated receptive field of the cell activated by the right eye remained unchanged following body tilt. In each case the displacement of the receptive field position results from a shift in the optic axes following body rotation. The results of this study corroborate the previous findingsS-S,10,16,17 that the receptive field properties of some cells in visual cortex are not immutable. In addition, some cortical cells, both in normally reared cats and in kittens raised under special conditions, appear to compensate for changes in head or body position. Similar space constancy effects have also been reported in the visual system of invertebrates. Visual receptive fields of certain fibers in the optic nerve of the crayfish are modified by changes in the animal's position in space 19. While orientation in space depends in large part upon visual cues, pertinent information is also supplied by input from vestibular receptors, from proprioceptors in joint capsules which provide data about the relative position of various parts of the body, as well as from cutaneous exteroceptors, particularly touch and pressure receptors. The experimental evidence relating to the modification of receptive field orientation during head or body tilt4,7,s,12,13,18 implies a role of visuovestibular convergence in perceptual constancy. Jung et al. 11 also suggest that vestibular afferents to visual cortex function to inform the visual system of body displacements. Perhaps the early stages of such visuovestibular integration may be seen in the properties of some of the cells described in this report. Moreover, such tilt-constant effects may provide a basis for certain psychophysical phenomena such as the apparent displacement of gravitational vertical in the direction opposite to sustained head tilt1, 3. This research was supported by NIMH Postdoctoral Fellowship 1 F02 MH44282-01 to JM, NIMH Grant F-R01 MH25329 to DNS, and NIH Grant 2 P50 NS10174. We thank J. K. Lane and N. Zolliker for technical assistance.
1 Aubert, H., Eine scheinbare bedeutende Drehung yon Objecten bei Neigung des Kopfes nach rechts oder links, Virchows Arch. path. Anat., 20 (1861) 381-393. 2 Bisti, S., Maffei, L. and Piccolino, M., Variations of the visual repsonses of the superior colliculus in relation to body roll, Science, 175 (1971) 456-457. 3 Day, R. H. and Wade, N. J., Visual spatial after-effect from prolonged head tilt, Science, 154 (1966) 1201-1202. 4 Denney, D. and Adorjani, C., Orientation specificity of visual cortical neurons after head tilt, Exp. Brain Res., 14 (1972) 312-317.
348 5 Hirsch, H. V. B. and Spinelli, D. N., Visual experience modifies distribution of horizontally and vertically oriented receptive fields in cats, Science, 168 (1970) 869-871. 6 Hirsch, H. V. B. and Spinelli, D. N., Modification of the distribution of receptive field orientation in cats by selective visual exposure during development, Exp. Brain Res., 13 (1971) 509 527. 7 Horn, G. and Hill, R. M., Modification of receptive fields of cells in the visual cortex occurring spontaneously and associated with bodily tilt, Nature (Lond.), 221 0969) 186-188. 8 Horn, G., Strechler, G. and Hill, R. M., Receptive fields of units in the visual cortex of the cat in the presence and absence of bodily tilt, Exp. Brain Res., 15 (1972) 113-132. 9 Hubel, D. H. and Wiesel, T. N., Receptive fields, binocular interaction and function architecture in the cat's visual cortex, J. Physiol. (Lond.), 160 (1962) 106-154. t0 Hubel, D. H. and Wiesel, T. N., Binocular interaction in striate cortex of kittens reared with artificial squint, J. Neurophysiol., 28 (1965) 1041-1059. 11 Jung, R., Kornhuber, H. H. and da Fonseca, J. S., Multisensory convergence on cortical neurons. In G. Moruzzi, A. Fessard and H. H. Jasper (Eds.), Brain Mechanisms, Progress in Brain Research, Vol. 1, Elsevier, Amsterdam, 1963, pp. 207 240. 12 Metzler, J. and Spinelli, D. N., Cortical development and perceptual invariance. In J. Metzler (Ed.), System Neuroscience, Academic Press, New York, 1977, pp. 25-54. 13 Metzler, J. and Spinelli, D. N., Tilt constancy mechanisms in kitten visual cortex, Neurosci. Abstr., 3 (1977) 569. 14 Otsuka, R. und Hassler, R., Uber Aufbau und Gliederung der corticalen Schsphare bei der Katze, Arch. Psyehiat. Nervenkr., 203 (1962) 212-234. 15 Spinelli, D. N., Receptive field organization of ganglion cells in the cat's retina, Exp. Neurol., 19 (1967) 291-315. 16 Spinelli, D. N., Recognition of visual patterns. In D. A. Hamburg, K. H. Pribram and A. J. Stunkard (Eds.), Perception and Its Disorders, (Association for Research in Nervous and Mental Disease, Research Publication, Vol. 48), Raven Press, New York, 1970, pp. 139-149. 17 Spinelli, D. N., Hirsch, H. V. B., Phelps, R. W. and Metzler, J., Visual experience as a determinant of the response characteristics of cortical receptive fields in cats, Exp. Brani Res., 15 (1972) 289-304. 18 Vakkur, G. J., Bishop, P. O. and Kozak, W., Visual optics in the cat, including posterior nodal distance and retinal landmarks, Vision Res., 3 (1963) 289-314. 19 Wiersma, C. A. G. and Yamaguchi, T., Integration of visual stimuli by the crayfish central nervous system, J. exp. Biol., 47 (1967) 409-431.
Brain Research, 163 (1979) 344-348 ~/Elsevier/North-Holland Biomedical Press
Tilt-constant receptive fields in the kitten visual cortex
JACQUELINE METZLER and D. NICO SPINELLI Department of Surgery, Section of Neurological Surgery, Yale University School of Medicine, New Haven, Conn. 06510 and Departments of Computer and Information Science and Psychology, University of Massachusetts, Amherst, Mass. 01003 (U.S.A.)
(Accepted November 9th, 1978)
Our perception of the visual world remains relatively constant during head or body tilt. Several recent reports4,7, 8,16 have suggested that, at least in the cat, this phenomenon of orientation or tilt-constancy might be explained by changes in the orientation specificity of about 5 ~ of the neurons in the visual cortex during head or body rotation. Units whose visual responses are modified by body tilt have also been found in the superior colliculusL Apparently, these cells all have dynamic visual properties. This report provides additional evidence that body tilt modifies the orientation specificity of certain neurons in the primary visual cortex. In an effort to examine the effects of early visual experience on the development of tilt-constant receptive fields, kittens were placed in a completely dark room from birth until 12-20 weeks of age. Beginning at 3.5 weeks of age, the kittens received daily selective visual stimulation. Each animal's total visual experience consisted of viewing a white field containing two black vertical bars with one eye while simultaneously viewing a white field with two black horizontal bars with other eye. The black bars were 1° wide and 13° long, with the center points 6 ° apart. The stimuli were mounted in goggles which the kittens wore for 4 h daily. The bars viewed by one eye were gravity-stabilized (i.e., they were free to rotate in the goggles) so that their orientation remained constant whenever the kitten tilted its head. The orthogonally oriented bars presented to the other eye were fixed in the goggles so that they maintained a constant orientation on the retina. In this way, each kitten served as its own control and the two effects could be conveniently compared. The stimuli were positioned in the goggles at the focal plane of a lens so that small changes in the position of the goggles would not affect the sharpness of focus. The eyepieces of the goggles provided a 50-60 ° field of view for each eye. Clear diffusing plastic near the ends of each eyepiece provided uniform illumination of the stimuli. The goggles were put on and removed inside the darkroom to insure that the animals received only the specified visual stimulation. The kittens quickly became accustomed to the goggles and behaved normally throughout the exposure periods. Records were taken from single units in area 17 when the kittens were between 12 and 20 weeks old. The preparation, recording and mapping techniques have been
345 described in detail in an earlier report lz. In brief, thiopental sodium (Pentothal) was injected intravenously to obtain surgical anesthesia. The kitten was placed in a stereotaxic apparatus and a small opening was made in the skin, bone and dura above the visual cortex of both hemispheres. All pressure points and incisions were infiltrated with a long-acting local anesthetic (Zyljectin). General anesthesia was then discontinued and the animal was immobilized with a continuous infusion of gallamine triethiodide (Flaxedil) (4.0 mg/kg/h) and artificially respired with a mixture of 70 N20-30 ~ 02 throughout the recording session. Core temperature was maintained at 37 ~ 1 °C. The kitten was placed 57 cm from a white tangent screen; at this distance 1 cm on the screen is equal to 1° visual angle. Contact lenses were used to correct for accommodation and protect the cornea of the eye. The optic discs were projected onto the screen with a reversible ophthalmoscope and the position of the area centralis inferred is. Electrode penetrations were made in area 17 between stereotaxic coordinates anterior-posterior --1.0 to + 1.0 mm and medial-lateral 0.5 to 1.5 mm. In the adult cat this corresponds to the region receiving projections from the area corresponds to the region receiving projections from the area centralis 14. Single-unit activity was recorded with tungsten microelectrodes. The receptive field of a cell was mapped with a black spot (1-4 ° in diameter) that was moved across a 25 ° by 25 ° white field by a computer-controlled x-y plotter. Unit activity was recorded at each of 2500 points within this field and presented on an oscilloscope screen as an integral contour display (see Fig. 1), thus displaying both the shape and the orientation of the receptive field. The general response characteristics, orientation selectivity and preferred direction of movement of each unit were also determined by manually moving light and dark bars, edges and spots across the visual field9. The receptive field of a cell was mapped when the kitten was in the standard (horizontal) position, when tilted 23 ° clockwise or counterclockwise, and again in the standard position. The shapes of the receptive fields of 94 units from the 8 kittens have been classified as either diffuse or elongated. Diffuse receptive fields have no clearly defined boundaries, with the units responding to stimulation over a large area of the visual field. Fifty-two units were of this type. One unit had a disc-shaped receptive field. The receptive fields of the remaining 41 units were classified as elongated. These units differed from those found in the normal cat in several respects: (1) they responded to input from only one eye. Normally, only 10-20 ~ of the cells in the visual cortex of the cat are monocularly activatedL As was anticipated, discordant stimulation of the two eyes resulted in a sharp reduction in binocularly driven units10; (2) when mapped with the kitten in the standard position, these units had receptive field orientations coincident with the bar pattern to which the eye had been exposed during rearing (see Fig. 1). In the normal cat, receptive fields of all orientations can be activated by both eyesg; (3) many of the elongated receptive fields were considerably larger than those of units receiving projections from the area centralis in normal cats 9. These results, however, are consistent with previously reported findings~,6,17. Barring any corrective factors, one would expect that when the immobilized animal is rotated about its longitudinal axis, the orientation of the receptive fields would rotate by the same amount and in the same direction, provided, of course, that
346
LE @
RE
J J
STANDARD ORIENTATION
TILTED CLOCKWISE 23 *
STANDARD ORIENTATION
Fig. 1. Integral contour displays of the receptive fields of two cells, each activated by a different eye. These cells were recorded from a kitten whose left eye had been exposed to two horizontal bars having a fixed retinal orientation and whose right eye had viewed two gravity-stabilized horizontal bars during development. The arrows designate the direction of stimulus movement during mapping.
one ensures that the eye remains stationary in the orbit. (The eyes were checked repeatedly throughout the experiment and caution was taken to eliminate eye movements with intravenous infusion of gallamine triethiodide and D-tubocurarine.) In this situation, the relationship between the head axis and the receptive field axis should remain constant. This is essentially what was observed for the receptive fields of those units that could be activated only by the eye that had viewed the pattern having a fixed retinal orientation during development. Upon returning the animal to the standard position, the fixed axis also returned to its original orientation. In other words, these receptive fields were not tilt-constant (Fig. 1). Twenty-two units were of this type. In contrast, the receptive field orientation of cells that could be activated only by the eye that had been exposed to the gravity-stabilized pattern during rearing
347 remained unchanged following body tilt, i.e., these cells appeared to demonstrate tiltconstancy. Nineteen units were of this classification. Integral contour displays of the receptive fields of two units - - one driven by the left eye and the other by the right eye - - are shown in Fig. 1. These units were recorded from a kitten exposed to two horizontal bars having a fixed retinal orientation with the left eye and two gravity-stabilized vertical bars with the right eye. The receptive fields of both cells were mapped when the kitten was in the standard position, when tilted 23° clockwise, and again in the standard position. Note that the two-bar receptive field - mimicking the stimulus pattern viewed during rearing - - was not tilt-constant, while the orientation of the vertically elongated receptive field of the cell activated by the right eye remained unchanged following body tilt. In each case the displacement of the receptive field position results from a shift in the optic axes following body rotation. The results of this study corroborate the previous findingsS-S,10,16,17 that the receptive field properties of some cells in visual cortex are not immutable. In addition, some cortical cells, both in normally reared cats and in kittens raised under special conditions, appear to compensate for changes in head or body position. Similar space constancy effects have also been reported in the visual system of invertebrates. Visual receptive fields of certain fibers in the optic nerve of the crayfish are modified by changes in the animal's position in space 19. While orientation in space depends in large part upon visual cues, pertinent information is also supplied by input from vestibular receptors, from proprioceptors in joint capsules which provide data about the relative position of various parts of the body, as well as from cutaneous exteroceptors, particularly touch and pressure receptors. The experimental evidence relating to the modification of receptive field orientation during head or body tilt4,7,s,12,13,18 implies a role of visuovestibular convergence in perceptual constancy. Jung et al. 11 also suggest that vestibular afferents to visual cortex function to inform the visual system of body displacements. Perhaps the early stages of such visuovestibular integration may be seen in the properties of some of the cells described in this report. Moreover, such tilt-constant effects may provide a basis for certain psychophysical phenomena such as the apparent displacement of gravitational vertical in the direction opposite to sustained head tilt1, 3. This research was supported by NIMH Postdoctoral Fellowship 1 F02 MH44282-01 to JM, NIMH Grant F-R01 MH25329 to DNS, and NIH Grant 2 P50 NS10174. We thank J. K. Lane and N. Zolliker for technical assistance.
1 Aubert, H., Eine scheinbare bedeutende Drehung yon Objecten bei Neigung des Kopfes nach rechts oder links, Virchows Arch. path. Anat., 20 (1861) 381-393. 2 Bisti, S., Maffei, L. and Piccolino, M., Variations of the visual repsonses of the superior colliculus in relation to body roll, Science, 175 (1971) 456-457. 3 Day, R. H. and Wade, N. J., Visual spatial after-effect from prolonged head tilt, Science, 154 (1966) 1201-1202. 4 Denney, D. and Adorjani, C., Orientation specificity of visual cortical neurons after head tilt, Exp. Brain Res., 14 (1972) 312-317.
348 5 Hirsch, H. V. B. and Spinelli, D. N., Visual experience modifies distribution of horizontally and vertically oriented receptive fields in cats, Science, 168 (1970) 869-871. 6 Hirsch, H. V. B. and Spinelli, D. N., Modification of the distribution of receptive field orientation in cats by selective visual exposure during development, Exp. Brain Res., 13 (1971) 509 527. 7 Horn, G. and Hill, R. M., Modification of receptive fields of cells in the visual cortex occurring spontaneously and associated with bodily tilt, Nature (Lond.), 221 0969) 186-188. 8 Horn, G., Strechler, G. and Hill, R. M., Receptive fields of units in the visual cortex of the cat in the presence and absence of bodily tilt, Exp. Brain Res., 15 (1972) 113-132. 9 Hubel, D. H. and Wiesel, T. N., Receptive fields, binocular interaction and function architecture in the cat's visual cortex, J. Physiol. (Lond.), 160 (1962) 106-154. t0 Hubel, D. H. and Wiesel, T. N., Binocular interaction in striate cortex of kittens reared with artificial squint, J. Neurophysiol., 28 (1965) 1041-1059. 11 Jung, R., Kornhuber, H. H. and da Fonseca, J. S., Multisensory convergence on cortical neurons. In G. Moruzzi, A. Fessard and H. H. Jasper (Eds.), Brain Mechanisms, Progress in Brain Research, Vol. 1, Elsevier, Amsterdam, 1963, pp. 207 240. 12 Metzler, J. and Spinelli, D. N., Cortical development and perceptual invariance. In J. Metzler (Ed.), System Neuroscience, Academic Press, New York, 1977, pp. 25-54. 13 Metzler, J. and Spinelli, D. N., Tilt constancy mechanisms in kitten visual cortex, Neurosci. Abstr., 3 (1977) 569. 14 Otsuka, R. und Hassler, R., Uber Aufbau und Gliederung der corticalen Schsphare bei der Katze, Arch. Psyehiat. Nervenkr., 203 (1962) 212-234. 15 Spinelli, D. N., Receptive field organization of ganglion cells in the cat's retina, Exp. Neurol., 19 (1967) 291-315. 16 Spinelli, D. N., Recognition of visual patterns. In D. A. Hamburg, K. H. Pribram and A. J. Stunkard (Eds.), Perception and Its Disorders, (Association for Research in Nervous and Mental Disease, Research Publication, Vol. 48), Raven Press, New York, 1970, pp. 139-149. 17 Spinelli, D. N., Hirsch, H. V. B., Phelps, R. W. and Metzler, J., Visual experience as a determinant of the response characteristics of cortical receptive fields in cats, Exp. Brani Res., 15 (1972) 289-304. 18 Vakkur, G. J., Bishop, P. O. and Kozak, W., Visual optics in the cat, including posterior nodal distance and retinal landmarks, Vision Res., 3 (1963) 289-314. 19 Wiersma, C. A. G. and Yamaguchi, T., Integration of visual stimuli by the crayfish central nervous system, J. exp. Biol., 47 (1967) 409-431.