- Email: [email protected]
Receptive field properties of neurons in the visual cortex of the rat
Neuroscience Letters, 27 ( 1981) 291-296
291
Elsevier/North-Holland Scientific Publishers Ltd.
RECEPTIVE FIELD PROPERTIES OF NEURONS IN THE VISUAL CORTEX OF THE RAT
JOHN G. PARNAVELAS, RICHARD A. BURNE and CHIA-S. LIN* Department of Cell Biology, The University of Texas Health Science Center at Dallas, 5323 Harry Hines Blvd., Dallas, TX 75235 (U.S.A.)
and *Department of Anatomy, Duke University, Durham, NC. 27710 (U.S.A.)
(Received August 28th, 1981; Revised version received October 6th, 1981; Accepted October 13th, 1981)
The receptive field properties of neurons were examined in the visual cortex, area 17, of Long-Evans pigmented rats. Visually responsive cells comprised 90o7oof cells recorded in area 17. Five percent of these cells responded only to stationary stimuli, while the remaining responded to both stationary and moving stimuli or only to movement. Cells of the latter category were classified as complex (44%), simple (27%), hypercomplex (13%) or non-oriented (16%). The results presented here show that, contrary to existing reports, neurons in the rat visual cortex have well-defined receptive field properties.
The rat is widely used in vision research, and recently detailed descriptions o f the cellular and synaptic organization o f the visual areas o f the brain, and in particular o f the visual cortex, have appeared in the literature [4, 12-14]. It is therefore surprising that, with the exception o f two qualitative and to some extent discordant studies [19, 22], there have been no systematic accounts o f the functional properties o f neurons in the visual cortex o f the rat. W e describe here the results o f a study utilizing both qualitative and quantitative analysis o f evoked spike activity o f single cells in area 17 o f the rat. Fifty L o n g - E v a n s pigmented rats ( 1 8 0 - 3 0 0 g) were used in this study. Animals were anesthetized with 2.5% h a l o t h a n e - o x y g e n gas mixture during surgical preparation and maintained at a 1% level during recording. The right visual cortex, area 17 [9], was exposed surgically and covered with 3% agar dissolved in Ringers' solution. The left eye was kept open with an adjustable metal ring and protected with clear silicone fluid. The pupil was left undilated and no corrective lenses were utilized since a recent study by H u g h e s [7] has suggested that the rat's eye is emmetropic. The extracellular spike activity o f single cortical neurons was recorded with glass microelectrodes ( 4 - 7 Mfl in situ) filled with F C F - F a s t Green Dye or 4 - 8 % horseradish peroxidase ( H R P ) . Unit activity, amplified and displayed with 0304-3940/81/0000-0000/$ 02.75 © Elsevier/North-Holland Scientific Publishers Ltd.
292
conventional electrophysical instrumentation, was converted into Schmitt-triggered pulses and entered into a Nova 3 computer (Data General Corporation) for poststimulus time and raster analysis. Visual stimuli, generated by a hand-held pentoscope and presented onto a tangent screen 30 cm from the animal [10], were used initially to characterize qualitatively response properties and localize approximate receptive field boundaries of 326 neurons. The response properties of 150 of these cells were analyzed quantitatively by presenting visual stimuli with an optical system controlled by a minicomputer. The visual stimuli, which were presented onto a dimly illuminated screen, consisted of stationary spots or bars of light of various sizes and moving bars of light of various widths and lengths. In some experiments, an attempt was made to impale individual neurons and inject them intracellularly with HRP after determining their response properties. The morphology of these physiologically identified neurons will be presented in a separate communication. At the completion of the recording, the animals were deeply anesthetized and perfused with fixative. Frozen sections were cut at 80-100 t~m in the coronal plane and stained in order to reconstruct electrode tracts. Visually responsive cell comprised approximately 90% (296/327) of the cells recorded in the visual cortex. The majority (95%) of these neurons responded to both stationary and moving stimuli or only to movement. The remaining cells responded only to stationary stimuli. Cells in the latter category were either oncenter, off-center or o n - o f f in type with the on-center cells predominating (9/15; 60%). The majority of cells that responded to movement were classified as complex, simple, hypercomplex or non-oriented on the basis of several criteria previously established for cells in the visual cortex of cat and monkey [3, 5, 8, 15, 17, 18, 20]. Complex cells were distinguished from simple cells by: (1) the spatial overlap of the activating regions evoked by a stimulus as it moved through the field in opposite directions; (2) the absence of inhibitory sidebands flanking the excitatory regions following conditioning test, and (3) the lack of summation of the responses as the stimulus increased in size within the excitatory regions of the receptive field. Complex cells comprised the majority of neurons that responded to moving stimuli (122/281; 44%). These cells, which tended to have an active background discharge rate, responded vigorously to a preferred stimulus generated by the handheld pentoscope or the computer. They preferred fast stimulus speeds (sometimes approaching 100°/sec) and displayed orientation and direction selectivities, although directional preference was absent in some cells. Fig. 1 illustrates the electrophysiological properties of one such complex cell. This cell displayed a tonic 'on' response at a latency of 68 msec to the presentation in the receptive field of a stationary rectangular bar (3.6 x 33.6 °; long axis horizontal) (Fig. la). Its response to a moving bar showed horizontal orientation preference but no noticeable direction selectivity (Fig. lb). Furthermore, presentation of a conditioning stimulus (light bar, 3 x 24 o) of varying velocities and orientations did not evoke inhibitory
293
off
on
:~£: ..:.:i ~":"' ': :.'.'".:. :""":""
..':
'.": ':"
:""
: ....
.'".
-"':i'-':-L
m me dl,,.,,,._itl~,,il~m.
•
•
5:'~;;; -.. ..
~ : . : - .
.
.
"'" . .
.
-3!
'.~:
~'.
M
Ilili[iIliJllJlllillilliiJlJliililllllllll t{{ll{llll{lllllllf{lllllllglg I 0.0 I ~,e 1 4e.O
_ . ~
.,m---L-m--{1
Illlllllrlllll r~4).O
I 8e.e
__
Fig. 1. a: raster and histogram illustrations of extracellular spike activity of a complex cell displaying an 'on' response to a stationary stimulus (light bar, 3.6 x 33.6 °) presented in the receptive field (0.2 Hz period) which was determined by a moving stimulus as shown in b; 15 sweeps, l0 msec bin width. Abscissa, 500 msec/division; ordinate, 30 spikes/sec, b: raster and histogram displays of evoked spike activity of the same neuron during movement of a bar at 72.1°/sec in the upward and downward directions. The upslope and the downslope segments of the trapezoid form shown at the top represent the upward and downward movement of the stimulus respectively. A conditioning stimulus (light bar 3 x 24 °) was presented at varying velocities and orientations. Excitation peaks for these movements have mean frequencies of 27.0 and 21.6 spikes/sec (12.1 and 5.6 spikes/sweep) for a temporal and spatial duration of 440 and 250 msec, and 33.1 and 18.3 ° respectively; 46 sweeps, 10 msec bin width. Abscissa, 500 msec/division; ordinate, 34.8 spikes/sec, c: histograms, corrected for response latency of 68 msec, of the evoked spike activity recorded in b during the upward (lower histogram) and downward (middle histogram) movements of the stimulus. The upper histogram includes both the upward (open bar) and downward (solid bar) movement histograms. Abscissa, degrees; ordinate, 34.8 spikes/sec.
s i d e b a n d s o n e i t h e r side o f t h e e x c i t a t o r y r e g i o n s (Fig. I b). E x p a n d e d h i s t o g r a m s o f t h e e v o k e d s p i k e a c t i v i t y r e c o r d e d d u r i n g t h e m o v e m e n t o f t h e s t i m u l u s in the o p p o s i t e d i r e c t i o n s d e m o n s t r a t e d s u p e r p o s i t i o n in s p a c e o f t h e t w o e x c i t a t o r y p e a k s (Fig. l c ) .
Simple cells ( 7 7 / 2 8 l ; 27°7o) u s u a l l y h a d l o w b a c k g r o u n d d i s c h a r g e r a t e , r e l a t i v e l y s m a l l r e c e p t i v e fields ( a p p r o x i m a t e l y movement
compared
5 - 1 5 °) a n d
preferred
slow velocities of
to t h e p r o p e r t i e s o f c o m p l e x cells. T h e m a j o r i t y d i s p l a y e d
294
ii
- :
. . . . .
...
.
.
.
.
-,'_
-
-
,-
a._X_i
i ',2.,;~ ~ ~ ~ ~ ', i ,~.,;~ ~ ', ~ ~ ', i ~.,;', ~ ~ ', ', ', i ,~.,;', : ', ', ~ ~ I
Fig. 2. a: raster and histogram displays of the extracellular spike activity of a simple cell responding to a moving bar (3.0 x 46.8 °) at 29.9°/sec in the upward and downward directions. The upslope and the downslope segments of the trapezoid form shown at the top represent the upward and downward movements of the stimulus respectively. A conditioning stimulus (light bar, 3 x 24 o) was presented at varying velocities and orientations. Note the presence of inhibitory sidebands (arrows). Excitation peaks have mean frequencies o f 22.1 and 19.8 spikes/sec (8.8 and 8.7 spikes/sweep), for a temporal and spatial duration of 380 and 420 msec, and l 1.0 ° and I 1.7 ° respectively; 27 sweeps, 18 msec bin width. Abscissa, 500 msec/division; ordinate, 26.7 spikes/sec, b: histograms constructed as described in Fig. lc to show the spatial separation of the cell illustrated in a without conditioning test. Approximate peak separation in 6.9°; abscissa in degrees.
strong orientation selectivity and their responses within the excitatory regions of the receptive field summated with increasing stimulus length and width. Fig. 2 illustrates properties of a simple cell in area 17 of the rat. The cell responded to a moving bar (3.0 x 46.8°; long axis horizontal) in the upward and downward directions. Histogram analysis revealed the presence of inhibitory sidebands (arrows; Fig. 2a) flanking the excitatory peaks following the presentation of a conditioning stimulus (light bar, 3 x 24°). In addition, expanded histograms of the spike activity evoked by the movement of the bar in opposite directions showed the spatial separation of the excitatory regions of the receptive field (Fig. 2b). Hypercomplex cells (32/281; 1307o) differed conspicuously from other cell types by the fact that they showed a striking reduction in response frequency ( > 6007o; see ref. 8) as an optimally oriented stimulus was elongated beyond the excitatory region of the receptive field. We noted in this study that, apart from length specificity, almost all hypercomplex cells encountered had the characteristic properties of either complex or simple cells. Finally, non-oriented cells comprised a distinct population (45/281; 16070) which responded to moving stimuli over a wide range of orientations. Neurons with non-oriented receptive field properties have been reported to comprise a substantial population in the visual cortex of rodents [2, 1l, 21, 22].
295 T o date, t w o r e p o r t s have d e s c r i b e d the receptive field p r o p e r t i e s o f n e u r o n s in the visual cortex o f the rat [19, 22]. W i e s e n f e l d a n d K o r n e l [22], b a s e d o n r e c o r d i n g s f r o m 107 n e u r o n s , r e p o r t e d t h a t n e u r o n s in the visual c o r t e x o f the h o o d e d rat were e q u a l l y d i v i d e d b e t w e e n cells r e s p o n d i n g to s t a t i o n a r y stimuli a n d those r e s p o n d i n g o n l y to m o v e m e n t . T h e m a j o r i t y o f cells in the latter c a t e g o r y were n o n - o r i e n t e d in type. In a similar s t u d y , Shaw et al. [19] r e p o r t e d t h a t a p p r o x i m a t e l y o n e - h a l f o f the cells they r e c o r d e d f r o m the visual c o r t e x o f the a l b i n o r a t (41/100) gave an ' i n d e f i n i t e ' r e s p o n s e to visual stimuli. T h e m a j o r i t y o f the r e m a i n i n g cells were c o m p l e x in type. These a u t h o r s d i d n o t i d e n t i f y a n y simple or h y p e r c o m p l e x cells in the rat visual cortex. C o n t r a r y to these r e p o r t s , the results p r e s e n t e d here clearly s h o w t h a t the m a j o r i t y o f n e u r o n s in the visual c o r t e x o f the rat have w e l l - d e f i n e d receptive field p r o p e r t i e s a n d r e s e m b l e t h o s e o f cells in the c o r r e s p o n d i n g cortex o f a n i m a l s with m o r e highly d e v e l o p e d visual systems [1, 5, 6, 16, 18, 20]. It a p p e a r s , t h e r e f o r e , t h a t a l t h o u g h the rat is p r e d o m i n a n t l y a n o c t u r n a l r o d e n t , single cells in the visual c o r t e x have f u n c t i o n a l capabilities similar to those in the c o r t e x o f the m o r e ' v i s u a l ' m a m m a l s . Differences in the p r e p a r a t i o n o f the a n i m a l s , a n e s t h e s i a a n d m e t h o d s o f d a t a collection a n d analysis m a y a c c o u n t for the d i s c r e p a n c y b e t w e e n o u r findings a n d the existing studies in the rat visual cortex. This s t u d y was s u p p o r t e d b y G r a n t s EY02964, DA02238, B N S 770174, a n d b y the Biological H u m a n i c s F o u n d a t i o n .
1 Chow, K.L., Masland, R.H. and Stewart, D.J., Receptive field characteristics of striate cortical neurons in the rabbit, Brain Res., 33 (1971) 337-352. 2 Dr~tger, U.C., Receptive fields of single cells and topography in mouse visual cortex, J. comp. Neurol., 160 0975) 269-290. 3 Dreher, B., Hypercomplex cells in the cat's striate cortex, Invest. Ophthalmol., ll (1972) 355-356. 4 Feldman, M.L. and Peters, A., The forms of non-pyramidal neurons in the visual cortex of the rat, J. comp. Neurol., 179 (1978) 761-794. 5 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. 6 Hubel, D.H. and Wiesel, T.N., Receptive fields and functional architecture of monkey striate cortex, J. Physiol. (Lond.), 195 (1968) 215-243. 7 Hughes, A., A schematic eye for the rat, Vision Res., (1979) 569-588. 8 Kato, H., Bishop, P.O. and Orban, G.A., Hypercomplex and simple/complex cell classifications in cat striate cortex, J. Neurophysiol., 41 (1978) 1071-1095. 9 Krieg, W.J.S., Connections of the cerebral cortex, I. The albino rat. A Topography of the cortical areas, J. comp. Neurol., 84 (1946) 221-276. 10 Lashley, K.S., The mechanism of vision. XIII. Cerebral function in discrimination of brightness when detail is controlled, J. comp. Neurol., 66 (1937) 471-490. I 1 Mangini, N.J. and Pearlman, A.L., Laminar distribution of receptive field properties in the primary visual cortex of the mouse, J. comp. Neurol., 193 (1980) 203-222. 12 Parnavelas, J.G., Lieberman, A.R. and Webster, K.E., Organization of neurons in the visual cortex, area 17, of the rat, J. Anat. (Lond.), 124 (1977) 305-322.
296 13 Parnavelas, J.G., Sullivan, K., Lieberman, A.R. and Webster, K.E., Neurons and their synaptic organization in the visual cortex of the rat. Electron microscopy of Golgi preparations, Cell Tiss. Res., 183 (1977) 499-517. 14 Peters, A. and Fairbn, A., Smooth and sparsely-spined stellate cells in the visual cortex of the rat: a study using a combined Golgi-electron microscope technique, J. comp. Neurol., 181 (1978) 129-172. 15 Pettigrew, J.D., Nikara, T. and Bishop, P.O., Responses to moving slits by single units in the cat striate cortex, Exp. Brain Res., 6 (1968) 373-390. 16 Rocha-Miranda, C.E., Linden, R., Volchan, E., Lent, R. and Bombardieri, R.A., Receptive field properties of single units in the opossum striate cortex, Brain Res., 104 (1976) 197-219. 17 Rose, D., The hypercomplex cell classification in the cat's striate cortex, J. Physiol. (Lond.), 242 (1974) 123-125P. 18 Schiller, P.H., Finlay, B.L. and Volman, S.F., Quantitative studies of single-cell properties in monkey striate cortex. I. Spatiotemporal organization of receptive fields, J. Neurophysiol., 39 (1976) 1288-1319. 19 Shaw, C., Yinon, U. and Auerbach, E., Receptive fields and response properties of neurons in the rat visual cortex, Vision Res., 15 (1975) 203-208. 20 Sherman, S.M., Watkins, D.W. and Wilson, J.R., Further differences in receptive field properties of simple and complex cells in the cat striate cortex, Vision Res., 16 (1976) 919-927. 21 Tiao, Y.-C. and Blakemore, C., Functional organization in the visual cortex of the golden hamster, J. comp. Neurol., 168 (1976) 459-482. 22 Wiesenfeld, Z. and Kornel, E.E., Receptive fields of single cells in the visual cortex of the hooded rat, Brain Res., 94 (1975) 401-412.
291
Elsevier/North-Holland Scientific Publishers Ltd.
RECEPTIVE FIELD PROPERTIES OF NEURONS IN THE VISUAL CORTEX OF THE RAT
JOHN G. PARNAVELAS, RICHARD A. BURNE and CHIA-S. LIN* Department of Cell Biology, The University of Texas Health Science Center at Dallas, 5323 Harry Hines Blvd., Dallas, TX 75235 (U.S.A.)
and *Department of Anatomy, Duke University, Durham, NC. 27710 (U.S.A.)
(Received August 28th, 1981; Revised version received October 6th, 1981; Accepted October 13th, 1981)
The receptive field properties of neurons were examined in the visual cortex, area 17, of Long-Evans pigmented rats. Visually responsive cells comprised 90o7oof cells recorded in area 17. Five percent of these cells responded only to stationary stimuli, while the remaining responded to both stationary and moving stimuli or only to movement. Cells of the latter category were classified as complex (44%), simple (27%), hypercomplex (13%) or non-oriented (16%). The results presented here show that, contrary to existing reports, neurons in the rat visual cortex have well-defined receptive field properties.
The rat is widely used in vision research, and recently detailed descriptions o f the cellular and synaptic organization o f the visual areas o f the brain, and in particular o f the visual cortex, have appeared in the literature [4, 12-14]. It is therefore surprising that, with the exception o f two qualitative and to some extent discordant studies [19, 22], there have been no systematic accounts o f the functional properties o f neurons in the visual cortex o f the rat. W e describe here the results o f a study utilizing both qualitative and quantitative analysis o f evoked spike activity o f single cells in area 17 o f the rat. Fifty L o n g - E v a n s pigmented rats ( 1 8 0 - 3 0 0 g) were used in this study. Animals were anesthetized with 2.5% h a l o t h a n e - o x y g e n gas mixture during surgical preparation and maintained at a 1% level during recording. The right visual cortex, area 17 [9], was exposed surgically and covered with 3% agar dissolved in Ringers' solution. The left eye was kept open with an adjustable metal ring and protected with clear silicone fluid. The pupil was left undilated and no corrective lenses were utilized since a recent study by H u g h e s [7] has suggested that the rat's eye is emmetropic. The extracellular spike activity o f single cortical neurons was recorded with glass microelectrodes ( 4 - 7 Mfl in situ) filled with F C F - F a s t Green Dye or 4 - 8 % horseradish peroxidase ( H R P ) . Unit activity, amplified and displayed with 0304-3940/81/0000-0000/$ 02.75 © Elsevier/North-Holland Scientific Publishers Ltd.
292
conventional electrophysical instrumentation, was converted into Schmitt-triggered pulses and entered into a Nova 3 computer (Data General Corporation) for poststimulus time and raster analysis. Visual stimuli, generated by a hand-held pentoscope and presented onto a tangent screen 30 cm from the animal [10], were used initially to characterize qualitatively response properties and localize approximate receptive field boundaries of 326 neurons. The response properties of 150 of these cells were analyzed quantitatively by presenting visual stimuli with an optical system controlled by a minicomputer. The visual stimuli, which were presented onto a dimly illuminated screen, consisted of stationary spots or bars of light of various sizes and moving bars of light of various widths and lengths. In some experiments, an attempt was made to impale individual neurons and inject them intracellularly with HRP after determining their response properties. The morphology of these physiologically identified neurons will be presented in a separate communication. At the completion of the recording, the animals were deeply anesthetized and perfused with fixative. Frozen sections were cut at 80-100 t~m in the coronal plane and stained in order to reconstruct electrode tracts. Visually responsive cell comprised approximately 90% (296/327) of the cells recorded in the visual cortex. The majority (95%) of these neurons responded to both stationary and moving stimuli or only to movement. The remaining cells responded only to stationary stimuli. Cells in the latter category were either oncenter, off-center or o n - o f f in type with the on-center cells predominating (9/15; 60%). The majority of cells that responded to movement were classified as complex, simple, hypercomplex or non-oriented on the basis of several criteria previously established for cells in the visual cortex of cat and monkey [3, 5, 8, 15, 17, 18, 20]. Complex cells were distinguished from simple cells by: (1) the spatial overlap of the activating regions evoked by a stimulus as it moved through the field in opposite directions; (2) the absence of inhibitory sidebands flanking the excitatory regions following conditioning test, and (3) the lack of summation of the responses as the stimulus increased in size within the excitatory regions of the receptive field. Complex cells comprised the majority of neurons that responded to moving stimuli (122/281; 44%). These cells, which tended to have an active background discharge rate, responded vigorously to a preferred stimulus generated by the handheld pentoscope or the computer. They preferred fast stimulus speeds (sometimes approaching 100°/sec) and displayed orientation and direction selectivities, although directional preference was absent in some cells. Fig. 1 illustrates the electrophysiological properties of one such complex cell. This cell displayed a tonic 'on' response at a latency of 68 msec to the presentation in the receptive field of a stationary rectangular bar (3.6 x 33.6 °; long axis horizontal) (Fig. la). Its response to a moving bar showed horizontal orientation preference but no noticeable direction selectivity (Fig. lb). Furthermore, presentation of a conditioning stimulus (light bar, 3 x 24 o) of varying velocities and orientations did not evoke inhibitory
293
off
on
:~£: ..:.:i ~":"' ': :.'.'".:. :""":""
..':
'.": ':"
:""
: ....
.'".
-"':i'-':-L
m me dl,,.,,,._itl~,,il~m.
•
•
5:'~;;; -.. ..
~ : . : - .
.
.
"'" . .
.
-3!
'.~:
~'.
M
Ilili[iIliJllJlllillilliiJlJliililllllllll t{{ll{llll{lllllllf{lllllllglg I 0.0 I ~,e 1 4e.O
_ . ~
.,m---L-m--{1
Illlllllrlllll r~4).O
I 8e.e
__
Fig. 1. a: raster and histogram illustrations of extracellular spike activity of a complex cell displaying an 'on' response to a stationary stimulus (light bar, 3.6 x 33.6 °) presented in the receptive field (0.2 Hz period) which was determined by a moving stimulus as shown in b; 15 sweeps, l0 msec bin width. Abscissa, 500 msec/division; ordinate, 30 spikes/sec, b: raster and histogram displays of evoked spike activity of the same neuron during movement of a bar at 72.1°/sec in the upward and downward directions. The upslope and the downslope segments of the trapezoid form shown at the top represent the upward and downward movement of the stimulus respectively. A conditioning stimulus (light bar 3 x 24 °) was presented at varying velocities and orientations. Excitation peaks for these movements have mean frequencies of 27.0 and 21.6 spikes/sec (12.1 and 5.6 spikes/sweep) for a temporal and spatial duration of 440 and 250 msec, and 33.1 and 18.3 ° respectively; 46 sweeps, 10 msec bin width. Abscissa, 500 msec/division; ordinate, 34.8 spikes/sec, c: histograms, corrected for response latency of 68 msec, of the evoked spike activity recorded in b during the upward (lower histogram) and downward (middle histogram) movements of the stimulus. The upper histogram includes both the upward (open bar) and downward (solid bar) movement histograms. Abscissa, degrees; ordinate, 34.8 spikes/sec.
s i d e b a n d s o n e i t h e r side o f t h e e x c i t a t o r y r e g i o n s (Fig. I b). E x p a n d e d h i s t o g r a m s o f t h e e v o k e d s p i k e a c t i v i t y r e c o r d e d d u r i n g t h e m o v e m e n t o f t h e s t i m u l u s in the o p p o s i t e d i r e c t i o n s d e m o n s t r a t e d s u p e r p o s i t i o n in s p a c e o f t h e t w o e x c i t a t o r y p e a k s (Fig. l c ) .
Simple cells ( 7 7 / 2 8 l ; 27°7o) u s u a l l y h a d l o w b a c k g r o u n d d i s c h a r g e r a t e , r e l a t i v e l y s m a l l r e c e p t i v e fields ( a p p r o x i m a t e l y movement
compared
5 - 1 5 °) a n d
preferred
slow velocities of
to t h e p r o p e r t i e s o f c o m p l e x cells. T h e m a j o r i t y d i s p l a y e d
294
ii
- :
. . . . .
...
.
.
.
.
-,'_
-
-
,-
a._X_i
i ',2.,;~ ~ ~ ~ ~ ', i ,~.,;~ ~ ', ~ ~ ', i ~.,;', ~ ~ ', ', ', i ,~.,;', : ', ', ~ ~ I
Fig. 2. a: raster and histogram displays of the extracellular spike activity of a simple cell responding to a moving bar (3.0 x 46.8 °) at 29.9°/sec in the upward and downward directions. The upslope and the downslope segments of the trapezoid form shown at the top represent the upward and downward movements of the stimulus respectively. A conditioning stimulus (light bar, 3 x 24 o) was presented at varying velocities and orientations. Note the presence of inhibitory sidebands (arrows). Excitation peaks have mean frequencies o f 22.1 and 19.8 spikes/sec (8.8 and 8.7 spikes/sweep), for a temporal and spatial duration of 380 and 420 msec, and l 1.0 ° and I 1.7 ° respectively; 27 sweeps, 18 msec bin width. Abscissa, 500 msec/division; ordinate, 26.7 spikes/sec, b: histograms constructed as described in Fig. lc to show the spatial separation of the cell illustrated in a without conditioning test. Approximate peak separation in 6.9°; abscissa in degrees.
strong orientation selectivity and their responses within the excitatory regions of the receptive field summated with increasing stimulus length and width. Fig. 2 illustrates properties of a simple cell in area 17 of the rat. The cell responded to a moving bar (3.0 x 46.8°; long axis horizontal) in the upward and downward directions. Histogram analysis revealed the presence of inhibitory sidebands (arrows; Fig. 2a) flanking the excitatory peaks following the presentation of a conditioning stimulus (light bar, 3 x 24°). In addition, expanded histograms of the spike activity evoked by the movement of the bar in opposite directions showed the spatial separation of the excitatory regions of the receptive field (Fig. 2b). Hypercomplex cells (32/281; 1307o) differed conspicuously from other cell types by the fact that they showed a striking reduction in response frequency ( > 6007o; see ref. 8) as an optimally oriented stimulus was elongated beyond the excitatory region of the receptive field. We noted in this study that, apart from length specificity, almost all hypercomplex cells encountered had the characteristic properties of either complex or simple cells. Finally, non-oriented cells comprised a distinct population (45/281; 16070) which responded to moving stimuli over a wide range of orientations. Neurons with non-oriented receptive field properties have been reported to comprise a substantial population in the visual cortex of rodents [2, 1l, 21, 22].
295 T o date, t w o r e p o r t s have d e s c r i b e d the receptive field p r o p e r t i e s o f n e u r o n s in the visual cortex o f the rat [19, 22]. W i e s e n f e l d a n d K o r n e l [22], b a s e d o n r e c o r d i n g s f r o m 107 n e u r o n s , r e p o r t e d t h a t n e u r o n s in the visual c o r t e x o f the h o o d e d rat were e q u a l l y d i v i d e d b e t w e e n cells r e s p o n d i n g to s t a t i o n a r y stimuli a n d those r e s p o n d i n g o n l y to m o v e m e n t . T h e m a j o r i t y o f cells in the latter c a t e g o r y were n o n - o r i e n t e d in type. In a similar s t u d y , Shaw et al. [19] r e p o r t e d t h a t a p p r o x i m a t e l y o n e - h a l f o f the cells they r e c o r d e d f r o m the visual c o r t e x o f the a l b i n o r a t (41/100) gave an ' i n d e f i n i t e ' r e s p o n s e to visual stimuli. T h e m a j o r i t y o f the r e m a i n i n g cells were c o m p l e x in type. These a u t h o r s d i d n o t i d e n t i f y a n y simple or h y p e r c o m p l e x cells in the rat visual cortex. C o n t r a r y to these r e p o r t s , the results p r e s e n t e d here clearly s h o w t h a t the m a j o r i t y o f n e u r o n s in the visual c o r t e x o f the rat have w e l l - d e f i n e d receptive field p r o p e r t i e s a n d r e s e m b l e t h o s e o f cells in the c o r r e s p o n d i n g cortex o f a n i m a l s with m o r e highly d e v e l o p e d visual systems [1, 5, 6, 16, 18, 20]. It a p p e a r s , t h e r e f o r e , t h a t a l t h o u g h the rat is p r e d o m i n a n t l y a n o c t u r n a l r o d e n t , single cells in the visual c o r t e x have f u n c t i o n a l capabilities similar to those in the c o r t e x o f the m o r e ' v i s u a l ' m a m m a l s . Differences in the p r e p a r a t i o n o f the a n i m a l s , a n e s t h e s i a a n d m e t h o d s o f d a t a collection a n d analysis m a y a c c o u n t for the d i s c r e p a n c y b e t w e e n o u r findings a n d the existing studies in the rat visual cortex. This s t u d y was s u p p o r t e d b y G r a n t s EY02964, DA02238, B N S 770174, a n d b y the Biological H u m a n i c s F o u n d a t i o n .
1 Chow, K.L., Masland, R.H. and Stewart, D.J., Receptive field characteristics of striate cortical neurons in the rabbit, Brain Res., 33 (1971) 337-352. 2 Dr~tger, U.C., Receptive fields of single cells and topography in mouse visual cortex, J. comp. Neurol., 160 0975) 269-290. 3 Dreher, B., Hypercomplex cells in the cat's striate cortex, Invest. Ophthalmol., ll (1972) 355-356. 4 Feldman, M.L. and Peters, A., The forms of non-pyramidal neurons in the visual cortex of the rat, J. comp. Neurol., 179 (1978) 761-794. 5 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. 6 Hubel, D.H. and Wiesel, T.N., Receptive fields and functional architecture of monkey striate cortex, J. Physiol. (Lond.), 195 (1968) 215-243. 7 Hughes, A., A schematic eye for the rat, Vision Res., (1979) 569-588. 8 Kato, H., Bishop, P.O. and Orban, G.A., Hypercomplex and simple/complex cell classifications in cat striate cortex, J. Neurophysiol., 41 (1978) 1071-1095. 9 Krieg, W.J.S., Connections of the cerebral cortex, I. The albino rat. A Topography of the cortical areas, J. comp. Neurol., 84 (1946) 221-276. 10 Lashley, K.S., The mechanism of vision. XIII. Cerebral function in discrimination of brightness when detail is controlled, J. comp. Neurol., 66 (1937) 471-490. I 1 Mangini, N.J. and Pearlman, A.L., Laminar distribution of receptive field properties in the primary visual cortex of the mouse, J. comp. Neurol., 193 (1980) 203-222. 12 Parnavelas, J.G., Lieberman, A.R. and Webster, K.E., Organization of neurons in the visual cortex, area 17, of the rat, J. Anat. (Lond.), 124 (1977) 305-322.
296 13 Parnavelas, J.G., Sullivan, K., Lieberman, A.R. and Webster, K.E., Neurons and their synaptic organization in the visual cortex of the rat. Electron microscopy of Golgi preparations, Cell Tiss. Res., 183 (1977) 499-517. 14 Peters, A. and Fairbn, A., Smooth and sparsely-spined stellate cells in the visual cortex of the rat: a study using a combined Golgi-electron microscope technique, J. comp. Neurol., 181 (1978) 129-172. 15 Pettigrew, J.D., Nikara, T. and Bishop, P.O., Responses to moving slits by single units in the cat striate cortex, Exp. Brain Res., 6 (1968) 373-390. 16 Rocha-Miranda, C.E., Linden, R., Volchan, E., Lent, R. and Bombardieri, R.A., Receptive field properties of single units in the opossum striate cortex, Brain Res., 104 (1976) 197-219. 17 Rose, D., The hypercomplex cell classification in the cat's striate cortex, J. Physiol. (Lond.), 242 (1974) 123-125P. 18 Schiller, P.H., Finlay, B.L. and Volman, S.F., Quantitative studies of single-cell properties in monkey striate cortex. I. Spatiotemporal organization of receptive fields, J. Neurophysiol., 39 (1976) 1288-1319. 19 Shaw, C., Yinon, U. and Auerbach, E., Receptive fields and response properties of neurons in the rat visual cortex, Vision Res., 15 (1975) 203-208. 20 Sherman, S.M., Watkins, D.W. and Wilson, J.R., Further differences in receptive field properties of simple and complex cells in the cat striate cortex, Vision Res., 16 (1976) 919-927. 21 Tiao, Y.-C. and Blakemore, C., Functional organization in the visual cortex of the golden hamster, J. comp. Neurol., 168 (1976) 459-482. 22 Wiesenfeld, Z. and Kornel, E.E., Receptive fields of single cells in the visual cortex of the hooded rat, Brain Res., 94 (1975) 401-412.