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A neuronal subsystem in the cat's area 18 lacks retinotopy
Brain Research, 410 (1987) 199-203
199
Elsevier BRE 22237
A neuronal subsystem in the cat's area 18 lacks retinotopy K. Albus A bteilung Neurobiologie, Max-Planck-lnstitut fiir Biophysikalische Chemie, GOttingen (F. R. G.) (Accepted 27 January 1987)
Key words: Area 18; Cat neocortex; Single neuron; Diffuse receptive field
Single neurones were recorded extracellularly in the visual cortex of anaesthetized and paralyzed cats. In all parts of area 18, neurones with diffuse receptive fields (DRFs) were found. DRFs measured at least 50° in diameter and always included the area centralis and large parts of the ipsi- and contralateral hemifeld; some DRFs even covered the entire visual field. DRF neurones gave phasic responses to diffuse light, and to light spots either presented stationary or moved rapidly across the field; they were not orientation- or direction-sensitive. In contrast to the majority of area 18 neurones, which are part of a retinotopically organized system, DRF neurones constitute a subsystem with only poor retinotopy, or no retinotopy at all. This system might be suitable for detecting sudden changes in global illumination.
A r e a 18, in the cat's n e o c o r t e x , has been shown to be retinotopically organized 3'15. M o r e recent studies have confirmed this observation and have revealed the details of the r e t i n o t o p y 1'5'14. In the course of our own extensive mappings of the occipital cortex, we occasionally r e c o r d e d from area 18 n e u r o n e s which did not fit in a retinotopic f r a m e w o r k . These neurones had receptive fields of an e x t r a o r d i n a r y large size often covering most of the entire visual field and were therefore t e r m e d ' n e u r o n e s with diffuse receptive fields ( D R F s ) ' . This r e p o r t presents data on the spatial organization of D R F s and the distribution of D R F neurones in a r e a 18. Twelve adult cats were used (weight 2 . 5 - 3 kg). A c c o r d i n g to p r o c e d u r e s described in detail elsewhere ~, the animals were anaesthetized with pentob a r b i t o n e ( N e m b u t a l , 35 mg/kg, i.p.) and anaesthesia was m a i n t a i n e d with a continuous infusion of pent o b a r b i t o n e ( 2 - 3 mg/kg/h) and by artificial ventilation with a mixture of N 2 0 / 0 2 / C 0 2 (72.5%/25%/ 2.5%). Muscular relaxation was induced with an initial injection of 20 mg, and m a i n t a i n e d by an infusion of gallamine triethiodide (Flaxedil, 40 mg/kg/h). Action potentials from single neurones were r e c o r d e d
extracellularly with tungsten-in-glass electrodes. The receptive fields were plotted on a p e r i m e t e r 0.5 m distant from the cat's eyes. The refractive errors were corrected with plastic contact lenses which had, in two cases, artificial pupils ( d i a m e t e r 3 mm). Action potentials and stimulus markers were displayed and stored on an oscilloscope screen and photographed. Visual stimulation was p r o d u c e d by projecting light-bars or spots from a light p r o j e c t o r operated by means of a c o m p u t e r - c o n t r o l l e d stimulation p r o g r a m m e , or with a hand-held lamp. Size and structure of D R F s were studied in detail in 22 neurones recorded from 4 animals (amongst which were the two cases with artificial pupils). F o r a further 60 neurones, recorded from the remaining 8 cats only the size of the D R F s and the position of D R F - n e u rones in area 18 were studied. The position of D R F neurones in area 18 was also studied from more than 100 unit clusters r e c o r d e d from all animals. The optimal stimulus for activating D R F - n e u r o n e s was a light white square of at least 10 ° in d i a m e t e r either p r e s e n t e d stationary or moved rapidly across the field. A consistent response was often elicited with a low contrast stimulus the intensity of which
Correspondence: K. Albus, Abteilung Neurobiologie, Max-Planck-Institut ffir Biophysikalische Chemic, Am Fassberg, D-3400 GOttingen, F.R.G. 0006-8993/87/$03.50 O 1987 Elsevier Science Publishers B.V. (Biomedical Division)
200 was 0.5 log unit or even less above background. A stationary square always elicited phasic responses (Figs. 1, 2) and by mapping DRFs systematically two receptive field types could be differentiated. Most neurones had uniform fields; i.e. they responded only to light ON (Fig. 1), or only to light OFF, or they gave only mixed ON/OFF responses. In addition neurones with compositefields were found. They had a subregion - - most frequently located in the centre of the field - - which responded differently to light patterns than the larger, surrounding region. The following centre-surround arrangements were obIpsil. Hemifie{d - ~ -
served: OFF centre and ON/OFF surround (Fig. 2), OFF centre and ON surround, or vice versa, and ON/OFF centre and ON surround. For these neurones diffuse light elicited either surround-type responses, or both surround- and centre-type responses. About 60% of all D R F neurones responded to stimulation of either eye and the remaining 40% to stimulation of one eye only. For binocular neurones, the sizes of the receptive fields usually differed between the two eyes (Fig.3). The figure also demonstrates that, as a rule, the DRFs included the area centralis and extended at least 15° into the ipsilateral 90°
- - ~ Control. H e m i f i e l d
60 ° HM
il~
-30 ° 30° VM
T
-30 °
Diffuse Light
I
I
80 ms
I
.D ms Fig. J. A neurone with diffuse receptive field from area 18. The main figure shows cell responses to light stimulation in restricted parts of the field. The sizes and the positions of the dark squares correspond to the sizes and positions of the light squares (30 ° x 30 °) used for stimulation. Within the dark squares, cell responses (one sweep) to light ON are reproduced. Sweep onset corresponds to stimulus onset. The ON-period of the stimulus lasted 2 s. The cell was driven only by the ipsilateral eye. Note that the latency of the ON-response was relatively short (less than 40 ms) when stimulating the right half of the field, or when stimulating with diffuse light (lower right inset). The extent of the DRF is shown in the upper right inset (hatched area). The cross hatched area indicates the average sizes and positions of receptive fields of other 'normal' cells recorded nearby. AC, area centralis; HM and VM, horizontal and vertical meridian. The dark dots indicate the positions of the blind spots.
201 90 ° Ipsi[. Hemifield ~ - -
--,,- Control. Hemifield
/ !
I
160 ms
3O~ ~
30 °
VM
_~o
'90 °
Pos. I
60 ° I
800 ms
I
Pos.1
Fig. 2. A neurone with a diffuse receptive field from area 18. The dark squares contain cell responses to light ON (underlined, top) and to light OFF (bottom). ON- and OFF-period, each lasted 0.8 s. Note the short latency of the OFF-response (less than 50 ms at most positions). The short latency OFF-response is followed by a long-latency secondary response (lower right inset). The extent of the DRF is shown in the upper right inset. Further explanations see text, and the legend to Fig. 1.
hemifield. O r i e n t a t i o n - and/or direction-sensitivity have not so far been o b s e r v e d in D R F neurones. D R F n e u r o n e s were e n c o u n t e r e d 500-1500 /xm below the pial surface and were found in all parts of a r e a 18. In areas 17 and 19 they were not seen. It is i m p o r t a n t to note that D R F neurones were always r e c o r d e d among o t h e r n e u r o n e s with smaller receptive fields of generally less than 20 ° across (see Figs. 1-3). This fact, as well as the use of artificial pupils in two cases, and the effectiveness of relatively low contrast stimuli, argues against stray light as a cause of D R F s . It also seems unlikely that D R F s are cortical representatives of the p e r i p h e r y - or shift-effect seen in the retina and the lateral geniculate b o d y 6'9. Firstly, D R F s do not have a subregion resembling the
'classic' receptive field of the retinal, lateral geniculate or cortical neurones. Secondly, the response amplitude of D R F neurones seems to be i n d e p e n d e n t of stimulus position (Figs. 1 and 2) whereas the shift effect decays with stimulus eccentricity 4"1°. Thirdly, the p e r i p h e r y effect disappears with subanaesthetic doses of barbiturates 9 whereas D R F s were routinely recorded in b a r b i t u r a t e - a n a e s t h e t i z e d animals. Even after an i.v. injection of an additional 10 mg pentobarbitone D R F neurones did not change their p r o p erties (3 neurones tested). In o r d e r to analyze possible contributions of afferent input to the p r o p e r t i e s of D R F neurones, the commissural input to one h e m i s p h e r e was blocked by making a d e e p parasagittal cut through the lateral gy-
202
A
HM
VM
VM
HM
VM
-HM
HM
VM
VM
HM
VM
~
VM
HM
HM
VM
HM
30 o
-HM
-HM
VM
-HM
-HM
!
VM
VM
I
30 ° VM
Fig. 3. Representative examples of diffuse receptive fields of area 18 neurones. A: DRFs of binocularly driven neurones; left column: ipsilateral receptive fields (RFs); right column: contralateral RFs. RFs belonging to each cell are arranged side by side. B: DRFs of monocularly driven neurones. Further explanation see legend of Fig. 1.
rus of the other hemisphere (two cases). Following this procedure, D R F neurones could be still recorded (Fig. 1). Undercutting areas 17-19 also did not change the frequency of occurrence of D R F neutones in the intact hemisphere 12. D R F s are certainly not produced by a convergence of ipsilateral afferent axons having restricted receptive fields, since cortical and subcortical afferents to
area 18 have been shown to be organized in a clear retinotopic fashion 2. Also, D R F s cannot be explained by the existence of large terminal arbors of Y-axons arising in the lateral geniculate body 8, since most D R F s cover more than a quarter of the visual field and all D R F s include the area centralis. On the other hand, neurones with diffuse receptive fields, in the lateral suprasylvian visual area 13 and in the nuo
203 cleus lateralis p o s t e r i o r of t h e t h a l a m u s 7, c o u l d well
lack of r e t i n o t o p y and its phasic r e s p o n s e b e h a v i o u r ,
r e p r e s e n t a d o m i n a n t i n p u t to D R F n e u r o n e s in a r e a
the s u b s y s t e m o f D R F n e u r o n e s w o u l d f u n c t i o n m o r e
18.
e f f e c t i v e l y in t h e d e t e c t i o n of s u d d e n c h a n g e s in g l o b -
A r e a 18 is s u p p o s e d to a n a l y z e and d e t e c t t h e posi-
al i l l u m i n a t i o n c a u s e d e i t h e r by m o v e m e n t o f the sur-
tions, f o r m s and in p a r t i c u l a r the m o v e m e n t o f spa-
r o u n d o r by the s u d d e n m o v e m e n t of the i m a g e dur-
tially r e s t r i c t e d light p a t t e r n s t°'n for which tasks
ing saccadic e y e m o v e m e n t s .
D R F n e u r o n e s w o u l d n o t be well suited. D u e to its
1 Albus, K. and Beckmann, R., Second and third visual areas of the cat: interindividual variability in retinotopic arrangement and cortical location, J. Physiol. (London), 299 (1980) 247-276. 2 Albus, K., Meyer, G. and Sanides, C.D., The retinotopy of cortical and subcortical areas projecting to the visual cortex (V1, V2, V3) of the cat, Exp. Brain Res., 41 (1980) A18. 3 Bilge, M., Bingle, A., Seneviratne, K.N. and Whineridge, D., A map of the visual cortex in the cat, J. Physiol. (London), 191 (1967) 116-118P. 4 Derrington, A.M., Lennie, P. and Wright, M.J., The mechanism of peripherally evoked responses in retinal ganglion cells, J. Physiol. (London), 289 (1979) 299-310. 5 Donaldson, J.M.L. and Whitteridge, D., The nature of the boundary between cortical visual areas II and III in the cat, Proc. R. Soc. London Ser. B, 199 (1977) 445-462. 6 Fischer, B., Krfiger, J. and Droll, W., Quantitative aspects of the shift-effect in cat retinal ganglion cells, Brain Research, 83 (1975) 391-403. 7 Godfraind, J.-M., Meulders, M. and Veraart, C., Visual properties of neurons in pulvinar, nucleus lateralis posterior and nucleus suprageniculatus thalami in the cat. I. Qualitative investigations, Brain Research, 44 (1972) 503-526. 8 Humphrey, A.L., Sur, M., Uhlrich, D.J. and Sherman, S.M., Termination patterns of individual X- and Y-cell ax-
9
10
11 12
13
14
15
ons in the visual cortex of the cat: projections to area 18, to the 17/18 border and to both areas 17 and 18, J. Comp. Neurol., 233 (1985) 190-212. Mcllwain, J.T., Receptive fields of optic tract axons and lateral geniculate cells: peripheral extent and barbiturate sensitivity, J. Neurophysiol., 27 (1964) 1154-1173. Orban, G.A., Area 18 of the cat: the first step in processing visual movement information, Perception, 6 (1977) 501-511. Orban, G.A. and Callens, M., Receptive field types of area 18 neurons in the cat, Exp. Brain Res., 30 (1977) 107-124. Sanides, D. and Albus, K., The distribution of interhemispheric projections in area 18 of the cat: coincidence with discontinuities of the representation of the visual field in the second visual area (V2), Exp. Brain Res., 38 (1980) 237-240. Spear, P.D. and Baumann, T.P., Receptive field characteristics of single neurons in lateral suprasylvian visual area of the cat, J. Neurophysiol., 38 (1975) 1403-1420. Tusa, R.J., Rosenquist, A.C. and Palmer, L.A., Retinotopic organization of areas 18 and 19 in cats, J. Comp. Neurol., 185 (1979) 657-678. Woolsey, C.N., Daube, J.P., Hoffmann, J., Kaas, J.H. and Ladpli, S., Representation of the visual field in visual areas I and II of the cat's cerebral cortex, Fed. Proc. Fed. Am. Soc. Exp. Biol., 26 (1967) 656.
199
Elsevier BRE 22237
A neuronal subsystem in the cat's area 18 lacks retinotopy K. Albus A bteilung Neurobiologie, Max-Planck-lnstitut fiir Biophysikalische Chemie, GOttingen (F. R. G.) (Accepted 27 January 1987)
Key words: Area 18; Cat neocortex; Single neuron; Diffuse receptive field
Single neurones were recorded extracellularly in the visual cortex of anaesthetized and paralyzed cats. In all parts of area 18, neurones with diffuse receptive fields (DRFs) were found. DRFs measured at least 50° in diameter and always included the area centralis and large parts of the ipsi- and contralateral hemifeld; some DRFs even covered the entire visual field. DRF neurones gave phasic responses to diffuse light, and to light spots either presented stationary or moved rapidly across the field; they were not orientation- or direction-sensitive. In contrast to the majority of area 18 neurones, which are part of a retinotopically organized system, DRF neurones constitute a subsystem with only poor retinotopy, or no retinotopy at all. This system might be suitable for detecting sudden changes in global illumination.
A r e a 18, in the cat's n e o c o r t e x , has been shown to be retinotopically organized 3'15. M o r e recent studies have confirmed this observation and have revealed the details of the r e t i n o t o p y 1'5'14. In the course of our own extensive mappings of the occipital cortex, we occasionally r e c o r d e d from area 18 n e u r o n e s which did not fit in a retinotopic f r a m e w o r k . These neurones had receptive fields of an e x t r a o r d i n a r y large size often covering most of the entire visual field and were therefore t e r m e d ' n e u r o n e s with diffuse receptive fields ( D R F s ) ' . This r e p o r t presents data on the spatial organization of D R F s and the distribution of D R F neurones in a r e a 18. Twelve adult cats were used (weight 2 . 5 - 3 kg). A c c o r d i n g to p r o c e d u r e s described in detail elsewhere ~, the animals were anaesthetized with pentob a r b i t o n e ( N e m b u t a l , 35 mg/kg, i.p.) and anaesthesia was m a i n t a i n e d with a continuous infusion of pent o b a r b i t o n e ( 2 - 3 mg/kg/h) and by artificial ventilation with a mixture of N 2 0 / 0 2 / C 0 2 (72.5%/25%/ 2.5%). Muscular relaxation was induced with an initial injection of 20 mg, and m a i n t a i n e d by an infusion of gallamine triethiodide (Flaxedil, 40 mg/kg/h). Action potentials from single neurones were r e c o r d e d
extracellularly with tungsten-in-glass electrodes. The receptive fields were plotted on a p e r i m e t e r 0.5 m distant from the cat's eyes. The refractive errors were corrected with plastic contact lenses which had, in two cases, artificial pupils ( d i a m e t e r 3 mm). Action potentials and stimulus markers were displayed and stored on an oscilloscope screen and photographed. Visual stimulation was p r o d u c e d by projecting light-bars or spots from a light p r o j e c t o r operated by means of a c o m p u t e r - c o n t r o l l e d stimulation p r o g r a m m e , or with a hand-held lamp. Size and structure of D R F s were studied in detail in 22 neurones recorded from 4 animals (amongst which were the two cases with artificial pupils). F o r a further 60 neurones, recorded from the remaining 8 cats only the size of the D R F s and the position of D R F - n e u rones in area 18 were studied. The position of D R F neurones in area 18 was also studied from more than 100 unit clusters r e c o r d e d from all animals. The optimal stimulus for activating D R F - n e u r o n e s was a light white square of at least 10 ° in d i a m e t e r either p r e s e n t e d stationary or moved rapidly across the field. A consistent response was often elicited with a low contrast stimulus the intensity of which
Correspondence: K. Albus, Abteilung Neurobiologie, Max-Planck-Institut ffir Biophysikalische Chemic, Am Fassberg, D-3400 GOttingen, F.R.G. 0006-8993/87/$03.50 O 1987 Elsevier Science Publishers B.V. (Biomedical Division)
200 was 0.5 log unit or even less above background. A stationary square always elicited phasic responses (Figs. 1, 2) and by mapping DRFs systematically two receptive field types could be differentiated. Most neurones had uniform fields; i.e. they responded only to light ON (Fig. 1), or only to light OFF, or they gave only mixed ON/OFF responses. In addition neurones with compositefields were found. They had a subregion - - most frequently located in the centre of the field - - which responded differently to light patterns than the larger, surrounding region. The following centre-surround arrangements were obIpsil. Hemifie{d - ~ -
served: OFF centre and ON/OFF surround (Fig. 2), OFF centre and ON surround, or vice versa, and ON/OFF centre and ON surround. For these neurones diffuse light elicited either surround-type responses, or both surround- and centre-type responses. About 60% of all D R F neurones responded to stimulation of either eye and the remaining 40% to stimulation of one eye only. For binocular neurones, the sizes of the receptive fields usually differed between the two eyes (Fig.3). The figure also demonstrates that, as a rule, the DRFs included the area centralis and extended at least 15° into the ipsilateral 90°
- - ~ Control. H e m i f i e l d
60 ° HM
il~
-30 ° 30° VM
T
-30 °
Diffuse Light
I
I
80 ms
I
.D ms Fig. J. A neurone with diffuse receptive field from area 18. The main figure shows cell responses to light stimulation in restricted parts of the field. The sizes and the positions of the dark squares correspond to the sizes and positions of the light squares (30 ° x 30 °) used for stimulation. Within the dark squares, cell responses (one sweep) to light ON are reproduced. Sweep onset corresponds to stimulus onset. The ON-period of the stimulus lasted 2 s. The cell was driven only by the ipsilateral eye. Note that the latency of the ON-response was relatively short (less than 40 ms) when stimulating the right half of the field, or when stimulating with diffuse light (lower right inset). The extent of the DRF is shown in the upper right inset (hatched area). The cross hatched area indicates the average sizes and positions of receptive fields of other 'normal' cells recorded nearby. AC, area centralis; HM and VM, horizontal and vertical meridian. The dark dots indicate the positions of the blind spots.
201 90 ° Ipsi[. Hemifield ~ - -
--,,- Control. Hemifield
/ !
I
160 ms
3O~ ~
30 °
VM
_~o
'90 °
Pos. I
60 ° I
800 ms
I
Pos.1
Fig. 2. A neurone with a diffuse receptive field from area 18. The dark squares contain cell responses to light ON (underlined, top) and to light OFF (bottom). ON- and OFF-period, each lasted 0.8 s. Note the short latency of the OFF-response (less than 50 ms at most positions). The short latency OFF-response is followed by a long-latency secondary response (lower right inset). The extent of the DRF is shown in the upper right inset. Further explanations see text, and the legend to Fig. 1.
hemifield. O r i e n t a t i o n - and/or direction-sensitivity have not so far been o b s e r v e d in D R F neurones. D R F n e u r o n e s were e n c o u n t e r e d 500-1500 /xm below the pial surface and were found in all parts of a r e a 18. In areas 17 and 19 they were not seen. It is i m p o r t a n t to note that D R F neurones were always r e c o r d e d among o t h e r n e u r o n e s with smaller receptive fields of generally less than 20 ° across (see Figs. 1-3). This fact, as well as the use of artificial pupils in two cases, and the effectiveness of relatively low contrast stimuli, argues against stray light as a cause of D R F s . It also seems unlikely that D R F s are cortical representatives of the p e r i p h e r y - or shift-effect seen in the retina and the lateral geniculate b o d y 6'9. Firstly, D R F s do not have a subregion resembling the
'classic' receptive field of the retinal, lateral geniculate or cortical neurones. Secondly, the response amplitude of D R F neurones seems to be i n d e p e n d e n t of stimulus position (Figs. 1 and 2) whereas the shift effect decays with stimulus eccentricity 4"1°. Thirdly, the p e r i p h e r y effect disappears with subanaesthetic doses of barbiturates 9 whereas D R F s were routinely recorded in b a r b i t u r a t e - a n a e s t h e t i z e d animals. Even after an i.v. injection of an additional 10 mg pentobarbitone D R F neurones did not change their p r o p erties (3 neurones tested). In o r d e r to analyze possible contributions of afferent input to the p r o p e r t i e s of D R F neurones, the commissural input to one h e m i s p h e r e was blocked by making a d e e p parasagittal cut through the lateral gy-
202
A
HM
VM
VM
HM
VM
-HM
HM
VM
VM
HM
VM
~
VM
HM
HM
VM
HM
30 o
-HM
-HM
VM
-HM
-HM
!
VM
VM
I
30 ° VM
Fig. 3. Representative examples of diffuse receptive fields of area 18 neurones. A: DRFs of binocularly driven neurones; left column: ipsilateral receptive fields (RFs); right column: contralateral RFs. RFs belonging to each cell are arranged side by side. B: DRFs of monocularly driven neurones. Further explanation see legend of Fig. 1.
rus of the other hemisphere (two cases). Following this procedure, D R F neurones could be still recorded (Fig. 1). Undercutting areas 17-19 also did not change the frequency of occurrence of D R F neutones in the intact hemisphere 12. D R F s are certainly not produced by a convergence of ipsilateral afferent axons having restricted receptive fields, since cortical and subcortical afferents to
area 18 have been shown to be organized in a clear retinotopic fashion 2. Also, D R F s cannot be explained by the existence of large terminal arbors of Y-axons arising in the lateral geniculate body 8, since most D R F s cover more than a quarter of the visual field and all D R F s include the area centralis. On the other hand, neurones with diffuse receptive fields, in the lateral suprasylvian visual area 13 and in the nuo
203 cleus lateralis p o s t e r i o r of t h e t h a l a m u s 7, c o u l d well
lack of r e t i n o t o p y and its phasic r e s p o n s e b e h a v i o u r ,
r e p r e s e n t a d o m i n a n t i n p u t to D R F n e u r o n e s in a r e a
the s u b s y s t e m o f D R F n e u r o n e s w o u l d f u n c t i o n m o r e
18.
e f f e c t i v e l y in t h e d e t e c t i o n of s u d d e n c h a n g e s in g l o b -
A r e a 18 is s u p p o s e d to a n a l y z e and d e t e c t t h e posi-
al i l l u m i n a t i o n c a u s e d e i t h e r by m o v e m e n t o f the sur-
tions, f o r m s and in p a r t i c u l a r the m o v e m e n t o f spa-
r o u n d o r by the s u d d e n m o v e m e n t of the i m a g e dur-
tially r e s t r i c t e d light p a t t e r n s t°'n for which tasks
ing saccadic e y e m o v e m e n t s .
D R F n e u r o n e s w o u l d n o t be well suited. D u e to its
1 Albus, K. and Beckmann, R., Second and third visual areas of the cat: interindividual variability in retinotopic arrangement and cortical location, J. Physiol. (London), 299 (1980) 247-276. 2 Albus, K., Meyer, G. and Sanides, C.D., The retinotopy of cortical and subcortical areas projecting to the visual cortex (V1, V2, V3) of the cat, Exp. Brain Res., 41 (1980) A18. 3 Bilge, M., Bingle, A., Seneviratne, K.N. and Whineridge, D., A map of the visual cortex in the cat, J. Physiol. (London), 191 (1967) 116-118P. 4 Derrington, A.M., Lennie, P. and Wright, M.J., The mechanism of peripherally evoked responses in retinal ganglion cells, J. Physiol. (London), 289 (1979) 299-310. 5 Donaldson, J.M.L. and Whitteridge, D., The nature of the boundary between cortical visual areas II and III in the cat, Proc. R. Soc. London Ser. B, 199 (1977) 445-462. 6 Fischer, B., Krfiger, J. and Droll, W., Quantitative aspects of the shift-effect in cat retinal ganglion cells, Brain Research, 83 (1975) 391-403. 7 Godfraind, J.-M., Meulders, M. and Veraart, C., Visual properties of neurons in pulvinar, nucleus lateralis posterior and nucleus suprageniculatus thalami in the cat. I. Qualitative investigations, Brain Research, 44 (1972) 503-526. 8 Humphrey, A.L., Sur, M., Uhlrich, D.J. and Sherman, S.M., Termination patterns of individual X- and Y-cell ax-
9
10
11 12
13
14
15
ons in the visual cortex of the cat: projections to area 18, to the 17/18 border and to both areas 17 and 18, J. Comp. Neurol., 233 (1985) 190-212. Mcllwain, J.T., Receptive fields of optic tract axons and lateral geniculate cells: peripheral extent and barbiturate sensitivity, J. Neurophysiol., 27 (1964) 1154-1173. Orban, G.A., Area 18 of the cat: the first step in processing visual movement information, Perception, 6 (1977) 501-511. Orban, G.A. and Callens, M., Receptive field types of area 18 neurons in the cat, Exp. Brain Res., 30 (1977) 107-124. Sanides, D. and Albus, K., The distribution of interhemispheric projections in area 18 of the cat: coincidence with discontinuities of the representation of the visual field in the second visual area (V2), Exp. Brain Res., 38 (1980) 237-240. Spear, P.D. and Baumann, T.P., Receptive field characteristics of single neurons in lateral suprasylvian visual area of the cat, J. Neurophysiol., 38 (1975) 1403-1420. Tusa, R.J., Rosenquist, A.C. and Palmer, L.A., Retinotopic organization of areas 18 and 19 in cats, J. Comp. Neurol., 185 (1979) 657-678. Woolsey, C.N., Daube, J.P., Hoffmann, J., Kaas, J.H. and Ladpli, S., Representation of the visual field in visual areas I and II of the cat's cerebral cortex, Fed. Proc. Fed. Am. Soc. Exp. Biol., 26 (1967) 656.