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Invariance of orientational and directional tuning in visual cortical cells of the adult cat
56
Brain Research, 96 (1975) 56-59 © Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
Invariance of orientational and directional tuning in visual cortical cells of the adult cat
P. HAMMOND, D. P. ANDREWS AND C. R. JAMES Research Department of Communication, University of Keele, Keele, Staffbrdshire ST5 5BG (Great Britain)
(Accepted May 28th, 1975)
Donaldson and Nash2, 3 have recently reported that the orientational and directional preferences of most cells in areas 17 and 18 of the adult cat vary with time. These results are at variance with those of numerous other groups throughout the world, notably those of Hubel and Wiese111,12, Bishop s,15, Henry s, Dreher 4,s,lv, Hoffmann 9, Barlow 1, Blakemore a,a6, Pettigrew 1,a~, Stoneg, 17, lkeda and Wright 13A4, and with our own extensive data which have been obtained over a number of years under a range of anaesthetic regimes and techniques of stimulation (refs. 5-7 and H a m m o n d and Andrews, in preparation). Even Horn and Hill's 1° claim of spontaneous modifications of cortical receptive fields involved shifts in orientation of only a few degrees and we therefore consider it worthwhile to make a brief report at this stage. Along with other properties, we have analysed the directional and orientational tuning of several hundred cells in areas 17 and t8 of the adult cat's visual cortex, whose receptive fields lay up to 15° from the projections of the areae centrales. The cats were prepared conventionally for visual experimentation. Pupils and nictitating membranes were retracted pharmacologically. Neutral contact lenses, together with 3 mm or 5 mm diameter artificial pupils, were employed routinely and 38 m m diameter trial lenses, selected retinoscopically, provided spherical correction for focus in the plane of a white tangent screen at 57 in. or 57 cm, or a Hewlett-Packard 1300A X-Y Display at 50 cm. The eyes were immobilised with an i.v. infusion of gallamine triethiodide (Flaxedil; May and Baker) in dextrose, usually coupled with bilateral cervical sympathectomy. Light anaesthesia - - pentobarbitone, chloralose, halothane-O2, 80 ~ :20 ~ N20-O2 ÷ halothane, 80 ~ :20 ~ NzO-O~ + trace pentobarbitone (averaging 1.0 mg/kg/h) - - was maintained throughout recording, with ventilation to 4 ~ end-tidal CO2 and monitoring of EEG, blood pressure and pulse, and rectal temperature. Cerveau isol6 preparations (rostro-pontine section) were used occasionally. Cell activity was recorded with low-impedance, 4 M NaC1- or Pontamine sky blue dye-filled micropipettes, and in many cases recording sites were confirmed histologically. Stimuli were hand-held wands, front or rear projection, or were
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Fig. 1. Orientational selectivity of (A) simple cell (107-HI) recorded in area 17 and (B) complex cell (114-K5) recorded in area 18 of the visual cortex of the adult cat, anaesthetised with 80%:20% N~O-O2 + trace pentobarbitone. Background luminance: +0.53 log cd/sq.m; 5 mm diameter artificial pupils. Moving bar stimuli were displayed on a computerised CRT display 50 cm in front of the animal. Each averaged response histogram shows the total responses to 15 sweeps of the stimulus (except in row 2, 20 sweeps). Each row shows the results of one experiment, during which the different orientations were interleaved in pseudorandom order. Stimulus orientation is shown in degrees beneath each histogram. Start time for each experiment on a given unit is shown at the right. Vertical scale: impulses per 20 msec bin (summed over 15 or 20 sweeps). Record duration, 2.0 sec (100 bins). The stimulus sweep duration was 1.5 sec for unit A and 2.0 sec for unit B, all movements in the preferred direction only.
generated o n a computer-controlled, X - Y display to be described in detail elsewhere (Andrews a n d H a m m o n d , in preparation). Cells from areas 17 a n d 18 were classified as simple, complex or lower-order hypercomplex (simple-type or complex-type) according to their p a t t e r n of discharge to m o v i n g stimuli; receptive field size; presence or absence of discrete, adjacent o n or off zones (if sensitive to flash); half-width of o r i e n t a t i o n a l t u n i n g ; sensitivity to bar l e n g t h ; s p o n t a n e o u s firing rate; preferred velocity and, more recently, responsiveness to r a n d o m l y textured visual noise4,6,a,gAl-lL M i n i m u m response fields 1 were d e t e r m i n e d for cells insensitive to flash, a n d recording depth, directional preference a n d ocular d o m i n a n c e were n o t e d routinely. The n o n - d o m i n a n t eye was invariably occluded, except for the few true b i n o c u l a r cells recorded in area 18 which gave n o response to m o n o c u l a r stimulation. Area 18 cells were distinguished from
58 those in area 17 by the stereotaxic coordinates of the recording site (including subsequent histology), receptive field size and preference for high velocities. Light or dark bars or edges were moved back and forth across the receptive field at orientations 3-12 ° apart. Orientational tuning curves were obtained for directionally selective cells, and for one or both directions in cells responsive (with or without bias) to two directions of motion 180° apart. The preferred orientation was invariably similar for both directions. In many cells sensitive to flashed stimuli, orientational tuning was also measured with stationary bars and, although it was our impression that such tuning curves tended to be narrower than those for moving stimuli, the optimal orientation was the same in each case. Particular care was always taken to ensure that bar width and velocity were optimal, that the stimulus path was centred over the receptive field, and that stimulus traverse and length were adequate to cover the field (with length limited at one or both ends in the case of hypercomplex cells). In numerous cells, several determinations of orientational tuning were made at varying intervals over periods up to 8 h. Fig. 1 illustrates examples of simple and complex cells recorded in areas 17 and 18, under 80~:20~o N20-O2 + trace pentobarbitone anaesthesia, using the computer-controlled X-Y display to interleave orientations in pseudorandom order. It is usually possible to distinguish simple and complex cells by the shape and span of their average response histograms, although in this respect the illustrated units are not good examples. However, in their invariance for orientation, the results illustrated are typical of those we have obtained under all anaesthetic regimes, regardless of technique of stimulation. Responsiveness varied in all types of preparation, as exemplified by Fig. 1, but in no instance have we observed shifts in orientational preference of more than a few degrees (i.e., within experimental error); nor have we seen dramatic shifts in directional bias, except in experiments involving interacting stimuli. These results are in line with those of numerous other researchers in the field, in antithesis to those of Donaldson and Nash 2,3, and we conclude that gross shifts of orientational and directional tuning are not features of cells in areas 17 and 18 of the adult cat. We believe that Donaldson and Nash's result may be due to a variety of factors which include excessively deep pentobarbitone anaesthesia leading to a cortex in which the responsiveness of units is abnormally low, the frequent use of binocular stimulation without correction of interocular alignment, and the coarseness of measurements of orientational tuning (made only at 45 ° spacings). C.R.J. is supported by M.R.C. Grant G.973/864. We thank Brian Whitehouse, Duncan Corbett and Hazel Henry for invaluable technical and secretarial assistance.
1 BARLOW,H. B., BLAKEMORE,C., AND PETTIGREW, J. D., The neural mechanism of binocular depth
discrimination, J. Physiol. (Lond.), 193 0967) 327-342. 2 DONALDSON, ]. M. L., AND NASH, J. R. G., Variability of properties of units in cat visual cortex,
J. Physiol. (Lond.), 230 (1973) 40~lP.
59 3 DONALDSON, I. M. L., AND NASH, J. R. G., Variability of the relative preference for stimulus orientation and direction of movement in some units of the cat visual cortex (areas 17 and 18), J. Physiol. (Lond.), 245 (1975) 305-324. 4 DREm:.R, B., Hypercomplex cells in the cat's striate cortex, Invest. Ophthal., 11 (1972) 355-356. 5 HAMMOND,P., Chromatic sensitivity and spatial organization of cat visual cortical cells: conerod interaction, J. Physiol. (Lond.), 213 (1971) 475-494. 6 HAMMOND,P., AND MACKAY, D. M., Differential responses of cat visual cortical cells to textured stimuli, Exp. Brain Res., 22 (1975) 427-430. 7 HAMMOND,P., ANDREWS, O. P., AND JAMES, C. R., Absence of spontaneous variability of orientational and directional tuning in cat visual cortical cells, J. Physiol. (Lond.), in press. 8 HENRY,G. H., BISHOP,P. O., TUPPER, R. M., ANDI)~EHER, B., Orientation specificity and response variability of cells in the striate cortex, Vision Res., 13 (1973) 1771-1779. 9 HOFFMANN,K.-P., AND STONE, J., Conduction velocity of afferents to cat visual cortex: a correlation with cortical receptive field properties, Brain Research, 32 (1971) 460-466. 10 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 (1969) 186-188. 11 HUBEL, D. 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. 12 HUBEL, D. H., AND WIESEL,T. N., Receptive fields and functional architecture in two non-striate visual areas (18 and 19) of the cat, J. Neurophysiol., 28 (1965) 229-289. 13 IKEDA, H., AND WRIGHT, M. J., Sensitivity of neurones in visual cortex (area 17) under different levels of anaesthesia, Exp. Brain Res., 20 (1974) 471-484. 14 IKEDA, H., AND WRIGHT, M. J., Retinotopic distribution, visual latency and orientation tuning of 'sustained' and 'transient' cortical neurones in area 17 of the cat, Exp. Brain Res., 22 (1975) 385-398. 15 PETTIGREW,J. D., NIKARA,T., AND BISHOP, P. O., Responses to moving slits by single units in cat striate cortex, Exp. Brain Res., 6 (1968) 373-390. 16 ROSE, D., AND BLAKEMORE,C., An analysis of orientation selectivity in the cat's visual cortex, Exp. Brain Res., 20 (1974) 1-17. 17 STONE,J., AND DREHER, B., Projection of X- and Y-cells of the cat's lateral geniculate nucleus to areas 17 and 18 of visual cortex, J. Neurophysiol., 36 (1973) 551-567.
Brain Research, 96 (1975) 56-59 © Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
Invariance of orientational and directional tuning in visual cortical cells of the adult cat
P. HAMMOND, D. P. ANDREWS AND C. R. JAMES Research Department of Communication, University of Keele, Keele, Staffbrdshire ST5 5BG (Great Britain)
(Accepted May 28th, 1975)
Donaldson and Nash2, 3 have recently reported that the orientational and directional preferences of most cells in areas 17 and 18 of the adult cat vary with time. These results are at variance with those of numerous other groups throughout the world, notably those of Hubel and Wiese111,12, Bishop s,15, Henry s, Dreher 4,s,lv, Hoffmann 9, Barlow 1, Blakemore a,a6, Pettigrew 1,a~, Stoneg, 17, lkeda and Wright 13A4, and with our own extensive data which have been obtained over a number of years under a range of anaesthetic regimes and techniques of stimulation (refs. 5-7 and H a m m o n d and Andrews, in preparation). Even Horn and Hill's 1° claim of spontaneous modifications of cortical receptive fields involved shifts in orientation of only a few degrees and we therefore consider it worthwhile to make a brief report at this stage. Along with other properties, we have analysed the directional and orientational tuning of several hundred cells in areas 17 and t8 of the adult cat's visual cortex, whose receptive fields lay up to 15° from the projections of the areae centrales. The cats were prepared conventionally for visual experimentation. Pupils and nictitating membranes were retracted pharmacologically. Neutral contact lenses, together with 3 mm or 5 mm diameter artificial pupils, were employed routinely and 38 m m diameter trial lenses, selected retinoscopically, provided spherical correction for focus in the plane of a white tangent screen at 57 in. or 57 cm, or a Hewlett-Packard 1300A X-Y Display at 50 cm. The eyes were immobilised with an i.v. infusion of gallamine triethiodide (Flaxedil; May and Baker) in dextrose, usually coupled with bilateral cervical sympathectomy. Light anaesthesia - - pentobarbitone, chloralose, halothane-O2, 80 ~ :20 ~ N20-O2 ÷ halothane, 80 ~ :20 ~ NzO-O~ + trace pentobarbitone (averaging 1.0 mg/kg/h) - - was maintained throughout recording, with ventilation to 4 ~ end-tidal CO2 and monitoring of EEG, blood pressure and pulse, and rectal temperature. Cerveau isol6 preparations (rostro-pontine section) were used occasionally. Cell activity was recorded with low-impedance, 4 M NaC1- or Pontamine sky blue dye-filled micropipettes, and in many cases recording sites were confirmed histologically. Stimuli were hand-held wands, front or rear projection, or were
57
A TIME 44
51
58
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60
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121 -9
-13
14 8 ~ ' ~ ""~~ : ~ -I
" .... -~.-:-:~:'~__ _.._S;'-L,=- ~ , - , - - -5
-9
-13
Fig. 1. Orientational selectivity of (A) simple cell (107-HI) recorded in area 17 and (B) complex cell (114-K5) recorded in area 18 of the visual cortex of the adult cat, anaesthetised with 80%:20% N~O-O2 + trace pentobarbitone. Background luminance: +0.53 log cd/sq.m; 5 mm diameter artificial pupils. Moving bar stimuli were displayed on a computerised CRT display 50 cm in front of the animal. Each averaged response histogram shows the total responses to 15 sweeps of the stimulus (except in row 2, 20 sweeps). Each row shows the results of one experiment, during which the different orientations were interleaved in pseudorandom order. Stimulus orientation is shown in degrees beneath each histogram. Start time for each experiment on a given unit is shown at the right. Vertical scale: impulses per 20 msec bin (summed over 15 or 20 sweeps). Record duration, 2.0 sec (100 bins). The stimulus sweep duration was 1.5 sec for unit A and 2.0 sec for unit B, all movements in the preferred direction only.
generated o n a computer-controlled, X - Y display to be described in detail elsewhere (Andrews a n d H a m m o n d , in preparation). Cells from areas 17 a n d 18 were classified as simple, complex or lower-order hypercomplex (simple-type or complex-type) according to their p a t t e r n of discharge to m o v i n g stimuli; receptive field size; presence or absence of discrete, adjacent o n or off zones (if sensitive to flash); half-width of o r i e n t a t i o n a l t u n i n g ; sensitivity to bar l e n g t h ; s p o n t a n e o u s firing rate; preferred velocity and, more recently, responsiveness to r a n d o m l y textured visual noise4,6,a,gAl-lL M i n i m u m response fields 1 were d e t e r m i n e d for cells insensitive to flash, a n d recording depth, directional preference a n d ocular d o m i n a n c e were n o t e d routinely. The n o n - d o m i n a n t eye was invariably occluded, except for the few true b i n o c u l a r cells recorded in area 18 which gave n o response to m o n o c u l a r stimulation. Area 18 cells were distinguished from
58 those in area 17 by the stereotaxic coordinates of the recording site (including subsequent histology), receptive field size and preference for high velocities. Light or dark bars or edges were moved back and forth across the receptive field at orientations 3-12 ° apart. Orientational tuning curves were obtained for directionally selective cells, and for one or both directions in cells responsive (with or without bias) to two directions of motion 180° apart. The preferred orientation was invariably similar for both directions. In many cells sensitive to flashed stimuli, orientational tuning was also measured with stationary bars and, although it was our impression that such tuning curves tended to be narrower than those for moving stimuli, the optimal orientation was the same in each case. Particular care was always taken to ensure that bar width and velocity were optimal, that the stimulus path was centred over the receptive field, and that stimulus traverse and length were adequate to cover the field (with length limited at one or both ends in the case of hypercomplex cells). In numerous cells, several determinations of orientational tuning were made at varying intervals over periods up to 8 h. Fig. 1 illustrates examples of simple and complex cells recorded in areas 17 and 18, under 80~:20~o N20-O2 + trace pentobarbitone anaesthesia, using the computer-controlled X-Y display to interleave orientations in pseudorandom order. It is usually possible to distinguish simple and complex cells by the shape and span of their average response histograms, although in this respect the illustrated units are not good examples. However, in their invariance for orientation, the results illustrated are typical of those we have obtained under all anaesthetic regimes, regardless of technique of stimulation. Responsiveness varied in all types of preparation, as exemplified by Fig. 1, but in no instance have we observed shifts in orientational preference of more than a few degrees (i.e., within experimental error); nor have we seen dramatic shifts in directional bias, except in experiments involving interacting stimuli. These results are in line with those of numerous other researchers in the field, in antithesis to those of Donaldson and Nash 2,3, and we conclude that gross shifts of orientational and directional tuning are not features of cells in areas 17 and 18 of the adult cat. We believe that Donaldson and Nash's result may be due to a variety of factors which include excessively deep pentobarbitone anaesthesia leading to a cortex in which the responsiveness of units is abnormally low, the frequent use of binocular stimulation without correction of interocular alignment, and the coarseness of measurements of orientational tuning (made only at 45 ° spacings). C.R.J. is supported by M.R.C. Grant G.973/864. We thank Brian Whitehouse, Duncan Corbett and Hazel Henry for invaluable technical and secretarial assistance.
1 BARLOW,H. B., BLAKEMORE,C., AND PETTIGREW, J. D., The neural mechanism of binocular depth
discrimination, J. Physiol. (Lond.), 193 0967) 327-342. 2 DONALDSON, ]. M. L., AND NASH, J. R. G., Variability of properties of units in cat visual cortex,
J. Physiol. (Lond.), 230 (1973) 40~lP.
59 3 DONALDSON, I. M. L., AND NASH, J. R. G., Variability of the relative preference for stimulus orientation and direction of movement in some units of the cat visual cortex (areas 17 and 18), J. Physiol. (Lond.), 245 (1975) 305-324. 4 DREm:.R, B., Hypercomplex cells in the cat's striate cortex, Invest. Ophthal., 11 (1972) 355-356. 5 HAMMOND,P., Chromatic sensitivity and spatial organization of cat visual cortical cells: conerod interaction, J. Physiol. (Lond.), 213 (1971) 475-494. 6 HAMMOND,P., AND MACKAY, D. M., Differential responses of cat visual cortical cells to textured stimuli, Exp. Brain Res., 22 (1975) 427-430. 7 HAMMOND,P., ANDREWS, O. P., AND JAMES, C. R., Absence of spontaneous variability of orientational and directional tuning in cat visual cortical cells, J. Physiol. (Lond.), in press. 8 HENRY,G. H., BISHOP,P. O., TUPPER, R. M., ANDI)~EHER, B., Orientation specificity and response variability of cells in the striate cortex, Vision Res., 13 (1973) 1771-1779. 9 HOFFMANN,K.-P., AND STONE, J., Conduction velocity of afferents to cat visual cortex: a correlation with cortical receptive field properties, Brain Research, 32 (1971) 460-466. 10 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 (1969) 186-188. 11 HUBEL, D. 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. 12 HUBEL, D. H., AND WIESEL,T. N., Receptive fields and functional architecture in two non-striate visual areas (18 and 19) of the cat, J. Neurophysiol., 28 (1965) 229-289. 13 IKEDA, H., AND WRIGHT, M. J., Sensitivity of neurones in visual cortex (area 17) under different levels of anaesthesia, Exp. Brain Res., 20 (1974) 471-484. 14 IKEDA, H., AND WRIGHT, M. J., Retinotopic distribution, visual latency and orientation tuning of 'sustained' and 'transient' cortical neurones in area 17 of the cat, Exp. Brain Res., 22 (1975) 385-398. 15 PETTIGREW,J. D., NIKARA,T., AND BISHOP, P. O., Responses to moving slits by single units in cat striate cortex, Exp. Brain Res., 6 (1968) 373-390. 16 ROSE, D., AND BLAKEMORE,C., An analysis of orientation selectivity in the cat's visual cortex, Exp. Brain Res., 20 (1974) 1-17. 17 STONE,J., AND DREHER, B., Projection of X- and Y-cells of the cat's lateral geniculate nucleus to areas 17 and 18 of visual cortex, J. Neurophysiol., 36 (1973) 551-567.