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Organization of geniculate inputs to visual cortical cells in the cat
Cbwn Rex. Vol. 25. No. 3. pp 3%3M. 1985 Printed III Great Bntain. All rights resrned
Copkrighr
(
0041-6989 $5 S3.00 - 0 00 1983 Pergamon Press Ltd
ORGANIZATION OF GENICULATE INPUTS TO VISUAL CORTICAL CELLS IN THE CAT KEIJI NHK
Science and Technical
Research
TAXAKA
Laboratories.
Kinuta.
Setagaya-ku.
Tokyo,
I57 Japan
Abstract-Neuronal connectivity between a .geniculate cell and a striate cortical cell was examined by cross-correlograms between their impulse actlvlties. Delayed positive correlations were found in 82 pairs. and the onset delay of the positivity was short enough in 65 pairs to infer that the geniculate cell monosynaptically excited the cortical cell. These monosynaptic excitations were found in both simple and complex cells. By determining connectivity of a cortical cell with multiple geniculate cells. the convergence of X and Y geniculate cells and that of on-center and off-center geniculate cells was demonstrated in several striate cells. Striate cortex application
Lateral
geniculate
nucleus
Convergence
INTRODUCTION
Two main cell groups have been distinguished in the cat striate cortex according to the spatial organization of their receptive fields. “Simple” ceils have narrow receptive fields composed of separate subareas for “on” and “off” responses to stationary stimuli, whereas “complex” cells have relatively wide, rather uniform fields throughout which “on-off“’ responses are obtained (Hubel and Wiesel, 1959, 1962). They also differ in their selectivity to the stimulus width. their responsiveness to textured stimuli (Hammond and MacKay, 1975), and possibly their selectivity to the stimulus speed (Movshon, 1975). It was originally suggested that excitations from geniculate cells were first conveyed to simple cells and then serially from there to complex cells (Hubel and Wiesel, 1962). Although the inputs from simple cells could simply explain the orientation and width selectivities of complex cells despite the rather uniform receptive fields of complex cells, this serial model has been challenged by most of the following experiments. They have shown that the electrical stimulation of geniculate fibers elicits excitations in complex cells as fast as in simple cells, and propose a parallel model that geniculate fibers monosynaptically innervate both simple and complex cells (Hoffman and Stone, 1971; Toyama Ed al., 1973; Singer ef al., 1975; Bullier and Henry, 1979a). Although the analysis with electrical stimulation appears to be a direct method of investigating the problem, it has a serious disadvantage. Since the electrical stimulation elicits action potentials in many afTerent fibers synchronously, very weak connections with a large convergence may show a prominent effect by the summation of EPSPs. There remains a possibility that the direct connections from geniculate 357
Cross-correlation
analysis
Bicuculline
cells to complex cells are too weak to perform the function of conveying the visual signals. Another important but unsettled problem with respect to the geniculostriate connections is whether the parallel channels in the lateral geniculate nucleus are also kept separate in the striate cortex or whether they converge onto single striate cells. Geniculate cells have been classified into on-center and off-center cells, and each of them further in X and Y types. In the original serial model, the convergence of oncenter and off-center geniculate cells played an important role in constructing the receptive fields of simple cells, but this on-off convergence has not been examined directly (Hubel and Wiesel, 1962). Through the technique of electrical stimulation, striate cells’ connectivity with X and Y geniculate cells has been investigated by utilizing the fact that Y cells have faster conduction velocities than X cells. As the simplest parallel model, it was first proposed that X afferents innervated simple cells and Y aferents innervated complex cells (HofTman and Stone. 1971). However, later experiments have failed to substantiate such a simple hypothesis (Singer et al.. 1975: Bullier and Henry, l979b). This uncertainty might be caused from a large overlap of conduction velocity between X and Y arerent fibers (Cleland et al.. 1976; Wilson ef al., 1976). Another disadvantage of electrical stimulation is that it can hardly reveal the convergence of X and Y geniculate cells to single striate cells. Excitations by slow arerents may be masked under electrical stimulation by refractoriness or inhibition after excitations by fast afferents, even if the slow and fast afferents converge onto single striate cells. These problems in the geniculostriate neuronal connections are investigated in the present study by using two new methods. One is a cross-correlation
anaiysis
ofimpulw
actIvltl~s
simuit,lns0usl~
ra_vrdd
from
both a geniculdte cell and ;I strldte cell ~Tanaka, 1983b). Its advantages are: 1. c?nl> functionall> significant connections are detected: and 2. \lsual responses of the pre- and post-sknaptic cells and properties of the connection itself can be examined at the same time. The other technique IS a comparison of responses between geniculate cells and striate cells. combined with an iontophoretic application of bicuculline. a GABA antagonist. onto the striate cells (Tanaka, 1983b). The comparison becomes fruitful only when the prominent intra-cortical inhibition. tvhich otherLvise modifies responses of striate cells. is removed by the bicucullin application (Sillito. 1975b). >IETHODS
Strgen Detailed methods have been described elsewhere Briefly, adult cats (Tanaka, 1983~~ 1983b). triethiodide were immobilized with gallamine (10 mg/kg/hr) and artificially ventilated with N,O/OZ (70:30) with the end-tidal CO? at 4.5”;. A bilateral cervical sypathectomy complemented the muscle relaxant for the eye ball stabilization. Eyes were focused through lenses and artificial pupils 3 mm in diameter on a screen located at 229 or I I4 cm from them. White light stimuli 0.8 log unit brighter than the background (2.5-4cd/m’) were projected on the screen. Recording In the experiments with the correlation technique, extracellular unit recordings were made simultaneously in the striate cortex (steel electrodes through the intact dura) and in the layers A, Al and C of the dorsal lateral geniculate nucleus (glass electrodes). The receptive fields of sampled cells were mapped on the screen, and the geniculate electrode was replaced until the geniculate receptive field overlapped the cortical receptive field. The neuronal connectivity between a geniculate cell and a striate ceil was then examined by cross-correlograms of their impulse discharges during periodic photic stimuli. In the experiments with bicuculline application, a three-barrelled glass electrode was placed in the striate cortex. A sharpened tungsten wire projecting from one of the barrels was used for extracellular recording, while the other two barrels were used for the iontophoresis of bicuculline (5 mM in 165 mM NaCI). For the comparison, responses of geniculate cells were recorded in the same animals, but in different sessions of the experiments. Cell classificalion Criteria for the classification of striate cells were the following: (I) cells with relatively small receptive fields (0.3-2.1’ in width) composed of subareas for pure “on” or “off” responses to a stationary slit (0. I wide and l-33 long) were classified as simple type.
Geniculate cells were classified into X. 1’ &I w types. using :I combination of the cr>ntrast :e\ers;il stimulus. a standing contrast and moiiny rectangular gratings. X cells were characterized b) ;I null sustained responses and modulated reposition, sponses to any spatial frequency in the three tests respecti\,ely. kvhile Y cells kvere characterized b> the absence of null position. transient responses and unmodulated responses to tine gratings (EnrothCugell and Robson. 1966: Cleland (‘I U! 197I: Fukadu, 197 I). W cells \vere identified by nonconcentric receptive fields or by “sluggish” responses (Cleland VI ~1.. 1976; Wilson et (II.. 1976). RESULTS
The cross-correlation analysis of neuronal connections were carried out on 243 geniculate-striate cell pairs. which were selected so that geniculate on-center fields overlapped striate on areas or geniculate off-center fields overlapped striate ofl‘ areas. Since cross-correlograms were calculated during photic stimulation, they were routinely processed by the “shuffling and subtraction” operations to exclude a component of correlation due to co-activation of the two cells by the photic stimulation (Toyamn e( (II., 1981; Tanaka, 1983b). Eighty two pairs showed positive correlations with positive delay times, which demonstrate that discharges occurred in the striate cell after those in the geniculate cell. The pairs include X geniculate-simple tested). X (26i71, pairs with positivities,‘pairs geniculate-standard-complex ( I7/45). Y geniculatesimple (5;20), Y geniculate-standard-complex (20/33) and Y geniculate-special-complex cell pairs (1 I i29). However, none of I6 X geniculate-special-complex cell pairs sho\ved significant correlations. Figure i(A) shows a typical example of positive correlation. which was obtained between an on-center X geniculate cell and a simple cell. The positivity began at I.5 msec, reached a maximum at 1.8 msec, and then declined gradually for the succeeding several milliseconds. The time course of the positivities was similar in most of the pairs (66182); the positivity (rise time, ;1 maximum attained sharply 0.8 k 0.4 msec) and then decayed rather gradually (total duration. -1.8 + I .8 msec). This time course is similar to that of intracellularly recorded EPSPS. and
Organization of geniculate inputs
9 ms
B
I
-1
I
I
I
I
I
I
I
I
I
I
9ms
0
Fig. I. Delayed positive correlations between impulse discharges of a geniculate cell and those of a striate cell. (A) Correlogram obtained between an on-center X geniculate cell and a simple cell. (B) Correlogram between an off-center X geniculate cell and a simple cell.
359
so favours a model in which the geniculate cell innervates the striate cell by excitatory synapse. The positivities in the other 16 pairs (5 with simple cells, 9 with standard-complex cells and 2 with specialcomplex cells) have plateaus, which appear rather symmetrical in shape [Fig. l(B)]. These were also regarded as representing geniculostriate connections since they showed onset delay time, rise time and total duration similar to that of the assymmetrically shaped positivities. The onset delays of the positive correlations were distributed from 0.9 to 2.7 msec (Fig. 2). On the basis of the geniculostriate conduction time of geniculate impuses and the delay time at geniculostriate synapses, the delay times can be divided into (I) a monosynaptic range, (2) an intermediate undefinable range, and (3) a polysynaptic range, The border between the monosynaptic and intermediate ranges (2.3 and 1.9 ms for X and Y geniculate cells respectively, indicated by open arrows) represents the sum of the fastest geniculostriate conduction time and the shortest delay for disynaptic activation of striate cells, and the border between the intermediate and polysynpatic ranges (3.8 and 2.8 msec for X and Y ceils) represents the sum of the slowest geniculostriate conduction time and the largest delay for monosynaptic activation of striate cells (Stone and Dreher. 1973; Cleland ef al., 1976; Toyama rr al., 1974; Bullier and Henry, 1979a). The delay time was Y
number 10
of pairs A
0
C
0.9 1.6 2.7 3.6 0.9 1.6 2.7 ms Fig. 2. Frequency distribution of onset delay of the positive correlations, shown separately for each combination of X, Y geniculate cells and simple (S). standard-complex (st-Cx). special-complex (sp-Cx) cells. Dotted part indicates simple cells with one subarea. Open arrows indicate the border between a monosynaptic range and an intermediate indefinable range, and filled arrows that between the latter range and a polysynaptic range.
360
A genlculafe
cell
c
(,
-30
-1
,
,
striate
9
0
cell
ms
0 I.II 0
2
00
Fig. 3. Calculation of contribution of an individual geniculate input to responses of a striate cell. (A) Cross-correlogram between an on-center X geniculate cell and a simple cell. (B and C) Responses of the two cells to a moving light slit during the correlogram was calculated. Nc,Ns gives the contribution. the monosynaptic range for most (65/78) of the pairs and within the intermediate range in the remaining pairs (13/79). There were no pairs with delays in the polysynaptic range. Monosynaptic delays were equally common for simple (28/3l) and standard-complex cells (31/36), but relatively less common for special-complex cells (6/l I). Since the cross-correlograms were calculated in responses to photic stimuli, these results indicate that the monosynaptic excitatory connections from geniculate cells to complex cells, as well as those to simple cells, are functionally significant in conveying visual signals. within
Contribution
of incliridual geniculute
0.1 for simple cells and 0.03 for complex cells. Such small values of the contribution indicate a convergence of many geniculate cells to a striate cell. pav
A
. i-l
0
4
8
12
number 16
16
20%
”
inputs
To gain insight into the number of converging geniculate inputs to a striate cell (the convergence number), the contribution by individual geniculate cells to photic responses of striate cells was quantitatively estimated. Figure 3 demonstrates how to calculate the contribution, showing a composition of an on-center geniculate cell and a simple cell. The positive correlation shown in Fig. 3(A) was calculated between their responses to a moving light slit shown in Figs. 3(B) and (C). The total counts contained in the positivity above the baseline [NC, hatched area in Fig. 3(A)] estimate the number of impulses in the striate cell which were locked to impulse discharges in the geniculate cell. These cortical impulse discharges are regarded to be triggered by excitations from the geniculate cell. Its ratio to the total number of cortical impulses [Ns, hatched area in Fig. 3(C)] then gives the contribution of excitatory inputs from the geniculate cell to the response of the cell. The ratio (Nc/Ns) was 0.09 in this case. Figure 4 illustrates the distribution of the contribution during moving stimulation in 71 pairs. A moving slit, rather than a stationary slit, was used in order to activate all the geniculate inputs over the receptive field of the striate cell. Values are approx.
st-cx
sp-cx
r-l
8 12 16 20% 0 4 Fig. 4. Frequency distribution of the contribution during moving stimulation. Arrows indicate the mean for each histogram.
Organization of geniculate inputs
ON -center
OFF-cenrer
Fig. 5. Convergence of geniculate inputs to a striate cell. (A} receptive field organization of a simple cell. Dotted and hatched areas indicate on and off areas respectiveiy. (B) and (C) center fields of on-center geniculate cells (B) and those of off-center geniculate cells (C) which were sampled simultaneously with the simple ceil. The sufhxes indicate the genicuiate cells’ X-Y classification. Solid-line circles indicate the geniculate cells for which positive correlations were found. and the broken-line circles the cells with no correlation. (D), (E) and (F)-a similar experiment on a standard-complex cell.
More than 10 geniculate cells converge onto a simple cell. while more than 30 geniculate cells converge onto a complex cell. Since the distribution is singlemodal in each of the three histograms. it is unlikely that fewer genicufate ceils make major contributions while the other genicufate inputs raises the background excitability. Comwgence
of genicdate
361
off-center geniculate cells. this is the expected result of a technical limitation. Each of the 3 simple cells could be examined with only one set oT geniculate cells whose center fields overlapped the same subarea of the receptive field of the simple ceil. Figures 5(D-F) show the convergence to a standard-complex cell. Out of the nine geniculate cells sampled simultaneously with the complex cell, positive correlations were found for 2 on-center cells [cell 1. 3 in Fig. 5(E)] and 3 off-center cells (cell 5, 6, 8 in Fig. 5(F)]. Such an on-off convergence was revealed in j standard- and 1 special-complex cell. Although the on-off convergence was demonstrated in both simple and complex cells, there was a clear difference in the spatial organization of the two inputs between simple and complex cells. The oncenter and off-center inputs were overlapping on the receptive field of a complex cell, but were separated on the receptive field of a simple cell. Of the five converging geniculate inputs to the standard-complex cell illustrated in Figs SfD-F), two were classified as X type and the others as Y type. It was, therefore, demonstrated that the standardcomplex cell received converging inputs from X and Y geniculate cells. The two converging inputs to the simple cell illustrated in Figs SfA-C) were both classified as X type. The X-Y convergence was demonstrated in I simple and 3 standard-complex cells. All of the geniculate inputs revealed in specialcomplex cells were classified as Y type. Figure 6 ilfustrates an example, in that positive correlations ON-center
inputs to a single striate cell
The convergence of multiple geniculate inputs was also directly studied by the cross-correlation technique. A special interest is directed to whether or not the genicufate parallel channels, i.e. on-center and off-center cells or X and Y cells, converge to a single striate ceff. While a singfe striate cell was kept recorded, 3-19 genicufate cells were sampled in succession, and neuronaf connections were determined for each pair. Two to five geniculate inputs were demonstrated in 5 simple, 8 standard-complex and 3 special-complex cells. Figures S(A-C) show an example of convergence to a simple cell. Center fields of 2 on-center geniculate cells [cell I, Z in Fig, 5(B)] overlapped the on-area of the simple cell, and center fields of 3 off-center geniculate cells [cefl 3, 4, 5 in Fig. 5(C)] overlapped the off-area of the simple cell. Positive correlations were found in pairs with celf 2 and cell 3, which are indicated by solid circles. No significant correlations were observed in pairs with the remaining three genicufate cells. ft was thus demonstrated that the simple cell received converging inputs from on-center and off-center geniculate cells. Although the convergence in the other 4 simple cells was pure convergence from on-center geniculate cells or that from
2*__ /
\
: r:-, : \ \,‘I . -’
3:,; -\!jy 11:./ 4’ 0
__ /
I \
\
\
\ _ .&
1 10
J Fig. 6. Convergence of geniculate inputs to a specialcomplex cell. (A) Similar Fig. 5(B) and (E). (B) Similar to Fig. 5(C) and (F). Another W cell with on-off center field was sampled but no correlation was observed with it.
A
Fig. 7. Responses of a simple (A), (B) and (C)---three light
cell to stationary light stimuli before and during the bicuculline application. stimuli. (D). (E) and (F)---responses to the slits shown in (A), (B) and (C)
respectively. (G).
(H) and (I)--responses
with 5 of the I I Y geniculate cells, but none of the 4 X or 2 W geniculate cells.
were obtained with
On-off convergence IO simple cells receded citculline application
b!, bi-
Throughout the course of the cross-correlation study, two types of simple cells were reocgnized. The presentation of a single stationary slit showed two or three subareas in the receptive field of the cells
during the bicuculline
application.
of a major group. Responses elicited in these subareas were roughtly balanced as shown in Fig. 7(D) and (E) (l/l-l/3 by peak amplitude). A single slit could reveal only one subarea in the receptive field of the remaining simple cells [Fig. 8(D)]. However, when two relatively large slits were simultaneously presented on both sides of this area, the cells yielded excitatory responses. The sign of the response was opposite to the response of the central consisting
I ..::::. c . ;::::_ . . ::::::y:::: :::::. ::::.._ ::::::::::: :::::: ,...:::: Arp”n cl I 1 I
J
ps&j
]I*
l-----J
F
D NOR
-L--A
‘--3----
.L._.
-AT-----l-
BIG
u
Fig. 8. Responses of another
simple cell before and during the bicuculline
application.
Similar to Fig. 7
Organization
363
of _eeniculate inputs
subarea (Fig. S(E)]. Therefore, the receptive field of the latter cells could be expressed either by one subarea or by symmetrically arranged three subareas. To further investigate the organization of excitatory inputs in these two groups of simple cells, the interaction between the subareas was examined while inhibitory inputs to the simple cells were reduced through an iontophoretic application of an antagonistic agent of the inhibitory synapses. The previous studies showed that transmitters of the inhibitory synapses in the cat striate cortex were GABA and an application of bicuculline, a GABA antagonist. considerably reduced the stimulus selectivities of striate cells (Sillito, l975a, 1975b: Tsumoto et al., 1979). It was expected that responses of striate cells submissively reflected the sum of excitatory inputs from geniculate cells when intra-cortical inhibitions were excluded. During the bicuculline application, different interactions between the subareas were observed in the two groups of simple ceils. Receptive fields of striate cells were mapped with a stationary slit while bicuculline was withheld with negative currents (IS-20 nA). Thirty-two cells were classified as simple cells. The bicuculline application with positive currents (30-150 nA) successfully reduced the orientation selectivity in 25 of the 32 cells. The criterion was that the peak amplitude of their responses to a stationary long (> 5’) slit with an orientation orthogonal to the optimal become more than 50% of that to a slit with the optimal orientation. Accompanying this reduction of the orientation selectivity. the antagonism between the subareas diminished. Although no responses were evoked in normal condition by the stimuli which covered the whole receptive fields [Figs 7(F) and S(F). the bicuculline application released excitatory responses to the stimuli. On-off responses were evoked in the simple cells with two or three subareas [20 cells, Fig. 7(l)], while either on or off responses were evoked in the simple cells which showed one subarea to a single small slit [5 cells, Fig. 8(I)]. The sign of the responses evoked in the latter cells was the same as that of their responses in the central area. The manner in which the simple cell illustrated in Fig. 8 responded to the three kinds of stimuli during the bicuculline application is similar to that of oncenter geniculate cells. On-center geniculate cells show on discharges to a stimulus covering the center area of their receptive fields and off discharges to a stimulus coverging their surround fields, while weaker on discharges are displayed to a stimulus covering the whole part of their receptive fields (Hubel and Wiesel, 1961). Therefore, it is very likely that the simple cell received excitatory inputs exclusively from on-center geniculate cells. The off discharges evoked in its surround field might have their source in the surround excitations of the on-center geniculate inputs. If these off responses had come from off-center geniculate inputs, off discharges in
addition to on discharges should been evoked in the simple cell by the stimulus covering the whole receptive field [Fig. S(I)]. On the other hand. the on-off responses in the remaining simple cells to the stimulus covering the whole receptive field [Fig. 7(I)] suggest that these cells recieved converging on-center and off-center geniculate inputs. Although both center and surround excitations are displayed in Y geniculate cells to the diffuse light flashing (Tanaka. l983a), the surround excitations become negligible as the stimulus size decreases. The stimuli used in the present study to cover the whole receptive field of the simple cells were relatively small (2-3’ in size). Stimuli of such a size never evoked on-off discharges in Y geniculate cells (own observation). Moreover, these simple cells showed on-off discharges even to smaller stimuli located at the border between their subareas. It is improbable, therefore, that the on-off discharges of the simple cells came from on-off discharges of either on-center or off-center Y geniculate cells. DISCUSSION
The present study shows that lateral geniculate cells exert monosynaptic excitations on complex striate cells as well as on simple striate cells. These connections are functionally significant; the geniculate excitations contribute to discharges of striate cells in response to photic stimuli. The study further points out that the parallel channels in the lateral geniculate nucleus, i.e. X and Y cells or on-center and off-center cells are mixed in many individual striate cells. The striate cells can be divided into several groups depending on whether they receive mixed inputs or pure inputs, and on whether the mixed inputs are spatially overlapping or separated. The contribution of single geniculate inputs to responses of a striate cell was calculated during stimulation with a moving light slit. The values were smaller for complex cells (mean, 0.03) than for simple cells (mean, 0. I), which suggests that more geniculate cells converge to a complex cell than to a simple cell. However, a possibility that complex cells receive excitations from other cortical cells as well as from geniculate cells, is not denied in the present study. If the cortical excitatory inputs to complex cells are significantly strong, the convergence number of geniculate cells onto a complex cell may be smaller. The balance between geniculate excitations and cortical excitations in complex cells should be examined in the future. The convergence of 2-5 geniculate cells was actually demonstrated in I7 striate cells. The number of geniculate inputs revealed was relatively small when compared to those expected from the values of the contribution. This is natural in that only a limited number (3-19) of geniculate cells were sampled in pair with each of the striate cells. Because a significant portion of geniculate inputs to individual striate cells might be missed, even if only on-center or off-center
Sf
cx
SP,CX
Fig. 9. Models for the organization connections.
of genicuiostriate
inputs, or X or Y inputs were exclusively revealed in a striate cell, it is not possible to conclude that the striate cell receive pure converging inputs from these kinds of geniculate cells. The on-off convergence was actually demonstrated in one simple cell. The responses of simple cells during the bicuculline application suggest that this is commonly true for a major subgroup of simple cells. The remaining simple ceils receive pure on-center or pure off-center inputs. The latter cells might be viewed as simple cells in some of the previous studies (Hubel and Wiesel, 1959; Gilbert, 1977), while they might be distinguished as a unique class of striate cells in other studies (Toyama and Takeda. 1974; Toyama et ul.. 1981). The on-OK convergence was also revealed in major complex cells. The on inputs and off inputs to complex cells are spatially overlapping. while those to simple cells are separated. The convergence of X and Y geniculate inputs could be expected for single simple cells and single standard-complex cells, since it was found that both groups of striate cells, as each cell group, receive excitations from both X and Y cells. Special-complex cells may receive Y inputs exclusively. The X-Y was actually demonstrated in 3 convergence standard-complex cells and 1 simple cell. A previous study examined responses of simple cells during the bicuculline application in connection with a set of photic stimuli which differentiated excitations in X and Y geniculate cells, and indicated that most simple cells receive pure X inputs or pure Y inputs (Tanaka, 1983a). Therefore, the X-Y convergence may occur mainly in standard-complex cells. As illustrated in Fig. 9, the present study suggests that there are several parallel channels in the cat striate cortex. Cells in the different channels receive geniculate excitations in different ways. REFERENCES Bullier J. and Henry G. neurons in cat striate 1751-1263.
H. (1979) Ordinal position cortex. J. .Vertroplt,r.~iol.
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Enroth-Cugeil C. and Robson J. G. (lY66) The contr:lq scnsitiwt) of reundl Fanglion cells of the UI J fili,s~j/ Lontl. 187. 5 I T-552. Fukada 1.. ( 1371) Receptlte field organzanon of c;~t optic nerve fibers with special reference to conduction ceiocit> C.~.~ion Re.s. II. 209-226. Gilbert C. D. 11977) Laminar differences in receptlie held properties oisells in cat primary visual cortex. J. Pi:i~\io/.. Lond. 268, 39 I-4, I. Hammond P. ,ind \lacKay D. Xl. (1975J Dttl’erential rcsponses ofcat usual cortical cells to textured stimuli. ~.+p/ Brtrv~ Rrs. 22. lI!imJ31) HotTman K.-P. and Stone J. (IY7 I) Conducrlon \eloclt\ ot a&rents 10 cat \isual cortex: a correlation with co&al receptive feld propertIes. Brrrir~ Res. 32, 460466. Hubel D. H. and Wicscl T. N. (1959) Receptive fields of single neurones in the cat‘s striate cortex. J. Phi,rio/.. Land. 148, 57&5Y I Hubel D. H. and Wicsel T. N. (IY61) Integratlvc actmn m the cat’s lateral geniculate body. J. PI~~~siol.. Loml 155,
335-398. Hubel D. H. and W~rscl T. S. (lY61) Rcceptivc licldb. binocular interaction and functional architecture in the cat’s wual cortex. J. Ph~sioi.. Loncl. 160, 106-l 5-l Movshon J. ;\. (1975) The velocity tuning of single units in cat striate cortex. J. PI~,rsio/.. Land 249, -I-l5~6S. Sillito A. M. (1975) The effectiveness of bicuculline as an antagonist of GABA and visually evoked inhibition in the Cal’s striate cortex. J. PIf~sio~.. Lonrl. 250, 287-304 Mlito A. M. (1975) The contribution of inhibitory mcchanisms to the receptive field properties of neurones in the striate cortex of the cat. J. Ph~siol.. Loncl. 250, 305 329. Singer W.. Tretter F. and Cyander M. (1975) Oreanization of cat striate cortex: a correlation of receptive-geld properties with afferent and etrerent connections. J. .Vwrnplt~siol. 38, lOSo-- 1098. Stone J. and Dreher B. (IY73) Projection of X- and Y-cells of the cat’s lateral grniculate nucleus to areas I7 and I8 of visual c0rte.x. J. :\‘cwqd~~~.~io/.36, 551-567 Tanaka K. (1983) Distinct X- and Y-streams in the cat wsuul cortex revealed by bicuculline application. Rrczin Res. 265, 143-337. Tanaka K. (IYY3) Cross-correlation analysis of gcmcuiostriate neuronal relationships in cats. J. .Vrrtr~&~siol. 49, 1303-1318. Toyama K., Maekabva K. and Takeda T. (1973) An analysis of neuronal circuitry for two types of visual cortical neurones classified on the basis of their responses to photic stimuli. Brain Res. 61, 395-399. Toyama K.. Matsunami K.. Ohno T. and Tokashikl S. (1974) An intracellular study of neuronal organization in the Lisual cortex. Espl Brain Res. 21, 4566. Toyama K. and Takeda T. (1974) A unique class of cat‘s visual cortical cells that exhibit either ON or OFF excitation for stationary light slits and are responsive IO moving edge patterns. Bruin Res. 73, 35&355. Toyama K.. Kimura M. and Tanaka K. (I981 ) Crosscorrelation analysis of interneuronal connectivity in cat visual cortex. J .~ewupl~~sio~. 46, l9l-101. Wilson P. D.. Rowe M. H. and Stone J. (1976) Properliec of relay cells in cat’s lateral geniculate nucleus: a comparison of W-cells with X- and Y-cells J .\;~rrrr~/~lr~.vic~/. 39. 1193-1209
Copkrighr
(
0041-6989 $5 S3.00 - 0 00 1983 Pergamon Press Ltd
ORGANIZATION OF GENICULATE INPUTS TO VISUAL CORTICAL CELLS IN THE CAT KEIJI NHK
Science and Technical
Research
TAXAKA
Laboratories.
Kinuta.
Setagaya-ku.
Tokyo,
I57 Japan
Abstract-Neuronal connectivity between a .geniculate cell and a striate cortical cell was examined by cross-correlograms between their impulse actlvlties. Delayed positive correlations were found in 82 pairs. and the onset delay of the positivity was short enough in 65 pairs to infer that the geniculate cell monosynaptically excited the cortical cell. These monosynaptic excitations were found in both simple and complex cells. By determining connectivity of a cortical cell with multiple geniculate cells. the convergence of X and Y geniculate cells and that of on-center and off-center geniculate cells was demonstrated in several striate cells. Striate cortex application
Lateral
geniculate
nucleus
Convergence
INTRODUCTION
Two main cell groups have been distinguished in the cat striate cortex according to the spatial organization of their receptive fields. “Simple” ceils have narrow receptive fields composed of separate subareas for “on” and “off” responses to stationary stimuli, whereas “complex” cells have relatively wide, rather uniform fields throughout which “on-off“’ responses are obtained (Hubel and Wiesel, 1959, 1962). They also differ in their selectivity to the stimulus width. their responsiveness to textured stimuli (Hammond and MacKay, 1975), and possibly their selectivity to the stimulus speed (Movshon, 1975). It was originally suggested that excitations from geniculate cells were first conveyed to simple cells and then serially from there to complex cells (Hubel and Wiesel, 1962). Although the inputs from simple cells could simply explain the orientation and width selectivities of complex cells despite the rather uniform receptive fields of complex cells, this serial model has been challenged by most of the following experiments. They have shown that the electrical stimulation of geniculate fibers elicits excitations in complex cells as fast as in simple cells, and propose a parallel model that geniculate fibers monosynaptically innervate both simple and complex cells (Hoffman and Stone, 1971; Toyama Ed al., 1973; Singer ef al., 1975; Bullier and Henry, 1979a). Although the analysis with electrical stimulation appears to be a direct method of investigating the problem, it has a serious disadvantage. Since the electrical stimulation elicits action potentials in many afTerent fibers synchronously, very weak connections with a large convergence may show a prominent effect by the summation of EPSPs. There remains a possibility that the direct connections from geniculate 357
Cross-correlation
analysis
Bicuculline
cells to complex cells are too weak to perform the function of conveying the visual signals. Another important but unsettled problem with respect to the geniculostriate connections is whether the parallel channels in the lateral geniculate nucleus are also kept separate in the striate cortex or whether they converge onto single striate cells. Geniculate cells have been classified into on-center and off-center cells, and each of them further in X and Y types. In the original serial model, the convergence of oncenter and off-center geniculate cells played an important role in constructing the receptive fields of simple cells, but this on-off convergence has not been examined directly (Hubel and Wiesel, 1962). Through the technique of electrical stimulation, striate cells’ connectivity with X and Y geniculate cells has been investigated by utilizing the fact that Y cells have faster conduction velocities than X cells. As the simplest parallel model, it was first proposed that X afferents innervated simple cells and Y aferents innervated complex cells (HofTman and Stone. 1971). However, later experiments have failed to substantiate such a simple hypothesis (Singer et al.. 1975: Bullier and Henry, l979b). This uncertainty might be caused from a large overlap of conduction velocity between X and Y arerent fibers (Cleland et al.. 1976; Wilson ef al., 1976). Another disadvantage of electrical stimulation is that it can hardly reveal the convergence of X and Y geniculate cells to single striate cells. Excitations by slow arerents may be masked under electrical stimulation by refractoriness or inhibition after excitations by fast afferents, even if the slow and fast afferents converge onto single striate cells. These problems in the geniculostriate neuronal connections are investigated in the present study by using two new methods. One is a cross-correlation
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both a geniculdte cell and ;I strldte cell ~Tanaka, 1983b). Its advantages are: 1. c?nl> functionall> significant connections are detected: and 2. \lsual responses of the pre- and post-sknaptic cells and properties of the connection itself can be examined at the same time. The other technique IS a comparison of responses between geniculate cells and striate cells. combined with an iontophoretic application of bicuculline. a GABA antagonist. onto the striate cells (Tanaka, 1983b). The comparison becomes fruitful only when the prominent intra-cortical inhibition. tvhich otherLvise modifies responses of striate cells. is removed by the bicucullin application (Sillito. 1975b). >IETHODS
Strgen Detailed methods have been described elsewhere Briefly, adult cats (Tanaka, 1983~~ 1983b). triethiodide were immobilized with gallamine (10 mg/kg/hr) and artificially ventilated with N,O/OZ (70:30) with the end-tidal CO? at 4.5”;. A bilateral cervical sypathectomy complemented the muscle relaxant for the eye ball stabilization. Eyes were focused through lenses and artificial pupils 3 mm in diameter on a screen located at 229 or I I4 cm from them. White light stimuli 0.8 log unit brighter than the background (2.5-4cd/m’) were projected on the screen. Recording In the experiments with the correlation technique, extracellular unit recordings were made simultaneously in the striate cortex (steel electrodes through the intact dura) and in the layers A, Al and C of the dorsal lateral geniculate nucleus (glass electrodes). The receptive fields of sampled cells were mapped on the screen, and the geniculate electrode was replaced until the geniculate receptive field overlapped the cortical receptive field. The neuronal connectivity between a geniculate cell and a striate ceil was then examined by cross-correlograms of their impulse discharges during periodic photic stimuli. In the experiments with bicuculline application, a three-barrelled glass electrode was placed in the striate cortex. A sharpened tungsten wire projecting from one of the barrels was used for extracellular recording, while the other two barrels were used for the iontophoresis of bicuculline (5 mM in 165 mM NaCI). For the comparison, responses of geniculate cells were recorded in the same animals, but in different sessions of the experiments. Cell classificalion Criteria for the classification of striate cells were the following: (I) cells with relatively small receptive fields (0.3-2.1’ in width) composed of subareas for pure “on” or “off” responses to a stationary slit (0. I wide and l-33 long) were classified as simple type.
Geniculate cells were classified into X. 1’ &I w types. using :I combination of the cr>ntrast :e\ers;il stimulus. a standing contrast and moiiny rectangular gratings. X cells were characterized b) ;I null sustained responses and modulated reposition, sponses to any spatial frequency in the three tests respecti\,ely. kvhile Y cells kvere characterized b> the absence of null position. transient responses and unmodulated responses to tine gratings (EnrothCugell and Robson. 1966: Cleland (‘I U! 197I: Fukadu, 197 I). W cells \vere identified by nonconcentric receptive fields or by “sluggish” responses (Cleland VI ~1.. 1976; Wilson et (II.. 1976). RESULTS
The cross-correlation analysis of neuronal connections were carried out on 243 geniculate-striate cell pairs. which were selected so that geniculate on-center fields overlapped striate on areas or geniculate off-center fields overlapped striate ofl‘ areas. Since cross-correlograms were calculated during photic stimulation, they were routinely processed by the “shuffling and subtraction” operations to exclude a component of correlation due to co-activation of the two cells by the photic stimulation (Toyamn e( (II., 1981; Tanaka, 1983b). Eighty two pairs showed positive correlations with positive delay times, which demonstrate that discharges occurred in the striate cell after those in the geniculate cell. The pairs include X geniculate-simple tested). X (26i71, pairs with positivities,‘pairs geniculate-standard-complex ( I7/45). Y geniculatesimple (5;20), Y geniculate-standard-complex (20/33) and Y geniculate-special-complex cell pairs (1 I i29). However, none of I6 X geniculate-special-complex cell pairs sho\ved significant correlations. Figure i(A) shows a typical example of positive correlation. which was obtained between an on-center X geniculate cell and a simple cell. The positivity began at I.5 msec, reached a maximum at 1.8 msec, and then declined gradually for the succeeding several milliseconds. The time course of the positivities was similar in most of the pairs (66182); the positivity (rise time, ;1 maximum attained sharply 0.8 k 0.4 msec) and then decayed rather gradually (total duration. -1.8 + I .8 msec). This time course is similar to that of intracellularly recorded EPSPS. and
Organization of geniculate inputs
9 ms
B
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I
I
I
I
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Fig. I. Delayed positive correlations between impulse discharges of a geniculate cell and those of a striate cell. (A) Correlogram obtained between an on-center X geniculate cell and a simple cell. (B) Correlogram between an off-center X geniculate cell and a simple cell.
359
so favours a model in which the geniculate cell innervates the striate cell by excitatory synapse. The positivities in the other 16 pairs (5 with simple cells, 9 with standard-complex cells and 2 with specialcomplex cells) have plateaus, which appear rather symmetrical in shape [Fig. l(B)]. These were also regarded as representing geniculostriate connections since they showed onset delay time, rise time and total duration similar to that of the assymmetrically shaped positivities. The onset delays of the positive correlations were distributed from 0.9 to 2.7 msec (Fig. 2). On the basis of the geniculostriate conduction time of geniculate impuses and the delay time at geniculostriate synapses, the delay times can be divided into (I) a monosynaptic range, (2) an intermediate undefinable range, and (3) a polysynaptic range, The border between the monosynaptic and intermediate ranges (2.3 and 1.9 ms for X and Y geniculate cells respectively, indicated by open arrows) represents the sum of the fastest geniculostriate conduction time and the shortest delay for disynaptic activation of striate cells, and the border between the intermediate and polysynpatic ranges (3.8 and 2.8 msec for X and Y ceils) represents the sum of the slowest geniculostriate conduction time and the largest delay for monosynaptic activation of striate cells (Stone and Dreher. 1973; Cleland ef al., 1976; Toyama rr al., 1974; Bullier and Henry, 1979a). The delay time was Y
number 10
of pairs A
0
C
0.9 1.6 2.7 3.6 0.9 1.6 2.7 ms Fig. 2. Frequency distribution of onset delay of the positive correlations, shown separately for each combination of X, Y geniculate cells and simple (S). standard-complex (st-Cx). special-complex (sp-Cx) cells. Dotted part indicates simple cells with one subarea. Open arrows indicate the border between a monosynaptic range and an intermediate indefinable range, and filled arrows that between the latter range and a polysynaptic range.
360
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Fig. 3. Calculation of contribution of an individual geniculate input to responses of a striate cell. (A) Cross-correlogram between an on-center X geniculate cell and a simple cell. (B and C) Responses of the two cells to a moving light slit during the correlogram was calculated. Nc,Ns gives the contribution. the monosynaptic range for most (65/78) of the pairs and within the intermediate range in the remaining pairs (13/79). There were no pairs with delays in the polysynaptic range. Monosynaptic delays were equally common for simple (28/3l) and standard-complex cells (31/36), but relatively less common for special-complex cells (6/l I). Since the cross-correlograms were calculated in responses to photic stimuli, these results indicate that the monosynaptic excitatory connections from geniculate cells to complex cells, as well as those to simple cells, are functionally significant in conveying visual signals. within
Contribution
of incliridual geniculute
0.1 for simple cells and 0.03 for complex cells. Such small values of the contribution indicate a convergence of many geniculate cells to a striate cell. pav
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To gain insight into the number of converging geniculate inputs to a striate cell (the convergence number), the contribution by individual geniculate cells to photic responses of striate cells was quantitatively estimated. Figure 3 demonstrates how to calculate the contribution, showing a composition of an on-center geniculate cell and a simple cell. The positive correlation shown in Fig. 3(A) was calculated between their responses to a moving light slit shown in Figs. 3(B) and (C). The total counts contained in the positivity above the baseline [NC, hatched area in Fig. 3(A)] estimate the number of impulses in the striate cell which were locked to impulse discharges in the geniculate cell. These cortical impulse discharges are regarded to be triggered by excitations from the geniculate cell. Its ratio to the total number of cortical impulses [Ns, hatched area in Fig. 3(C)] then gives the contribution of excitatory inputs from the geniculate cell to the response of the cell. The ratio (Nc/Ns) was 0.09 in this case. Figure 4 illustrates the distribution of the contribution during moving stimulation in 71 pairs. A moving slit, rather than a stationary slit, was used in order to activate all the geniculate inputs over the receptive field of the striate cell. Values are approx.
st-cx
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8 12 16 20% 0 4 Fig. 4. Frequency distribution of the contribution during moving stimulation. Arrows indicate the mean for each histogram.
Organization of geniculate inputs
ON -center
OFF-cenrer
Fig. 5. Convergence of geniculate inputs to a striate cell. (A} receptive field organization of a simple cell. Dotted and hatched areas indicate on and off areas respectiveiy. (B) and (C) center fields of on-center geniculate cells (B) and those of off-center geniculate cells (C) which were sampled simultaneously with the simple ceil. The sufhxes indicate the genicuiate cells’ X-Y classification. Solid-line circles indicate the geniculate cells for which positive correlations were found. and the broken-line circles the cells with no correlation. (D), (E) and (F)-a similar experiment on a standard-complex cell.
More than 10 geniculate cells converge onto a simple cell. while more than 30 geniculate cells converge onto a complex cell. Since the distribution is singlemodal in each of the three histograms. it is unlikely that fewer genicufate ceils make major contributions while the other genicufate inputs raises the background excitability. Comwgence
of genicdate
361
off-center geniculate cells. this is the expected result of a technical limitation. Each of the 3 simple cells could be examined with only one set oT geniculate cells whose center fields overlapped the same subarea of the receptive field of the simple ceil. Figures 5(D-F) show the convergence to a standard-complex cell. Out of the nine geniculate cells sampled simultaneously with the complex cell, positive correlations were found for 2 on-center cells [cell 1. 3 in Fig. 5(E)] and 3 off-center cells (cell 5, 6, 8 in Fig. 5(F)]. Such an on-off convergence was revealed in j standard- and 1 special-complex cell. Although the on-off convergence was demonstrated in both simple and complex cells, there was a clear difference in the spatial organization of the two inputs between simple and complex cells. The oncenter and off-center inputs were overlapping on the receptive field of a complex cell, but were separated on the receptive field of a simple cell. Of the five converging geniculate inputs to the standard-complex cell illustrated in Figs SfD-F), two were classified as X type and the others as Y type. It was, therefore, demonstrated that the standardcomplex cell received converging inputs from X and Y geniculate cells. The two converging inputs to the simple cell illustrated in Figs SfA-C) were both classified as X type. The X-Y convergence was demonstrated in I simple and 3 standard-complex cells. All of the geniculate inputs revealed in specialcomplex cells were classified as Y type. Figure 6 ilfustrates an example, in that positive correlations ON-center
inputs to a single striate cell
The convergence of multiple geniculate inputs was also directly studied by the cross-correlation technique. A special interest is directed to whether or not the genicufate parallel channels, i.e. on-center and off-center cells or X and Y cells, converge to a single striate ceff. While a singfe striate cell was kept recorded, 3-19 genicufate cells were sampled in succession, and neuronaf connections were determined for each pair. Two to five geniculate inputs were demonstrated in 5 simple, 8 standard-complex and 3 special-complex cells. Figures S(A-C) show an example of convergence to a simple cell. Center fields of 2 on-center geniculate cells [cell I, Z in Fig, 5(B)] overlapped the on-area of the simple cell, and center fields of 3 off-center geniculate cells [cefl 3, 4, 5 in Fig. 5(C)] overlapped the off-area of the simple cell. Positive correlations were found in pairs with celf 2 and cell 3, which are indicated by solid circles. No significant correlations were observed in pairs with the remaining three genicufate cells. ft was thus demonstrated that the simple cell received converging inputs from on-center and off-center geniculate cells. Although the convergence in the other 4 simple cells was pure convergence from on-center geniculate cells or that from
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A
Fig. 7. Responses of a simple (A), (B) and (C)---three light
cell to stationary light stimuli before and during the bicuculline application. stimuli. (D). (E) and (F)---responses to the slits shown in (A), (B) and (C)
respectively. (G).
(H) and (I)--responses
with 5 of the I I Y geniculate cells, but none of the 4 X or 2 W geniculate cells.
were obtained with
On-off convergence IO simple cells receded citculline application
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Throughout the course of the cross-correlation study, two types of simple cells were reocgnized. The presentation of a single stationary slit showed two or three subareas in the receptive field of the cells
during the bicuculline
application.
of a major group. Responses elicited in these subareas were roughtly balanced as shown in Fig. 7(D) and (E) (l/l-l/3 by peak amplitude). A single slit could reveal only one subarea in the receptive field of the remaining simple cells [Fig. 8(D)]. However, when two relatively large slits were simultaneously presented on both sides of this area, the cells yielded excitatory responses. The sign of the response was opposite to the response of the central consisting
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Organization
363
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subarea (Fig. S(E)]. Therefore, the receptive field of the latter cells could be expressed either by one subarea or by symmetrically arranged three subareas. To further investigate the organization of excitatory inputs in these two groups of simple cells, the interaction between the subareas was examined while inhibitory inputs to the simple cells were reduced through an iontophoretic application of an antagonistic agent of the inhibitory synapses. The previous studies showed that transmitters of the inhibitory synapses in the cat striate cortex were GABA and an application of bicuculline, a GABA antagonist. considerably reduced the stimulus selectivities of striate cells (Sillito, l975a, 1975b: Tsumoto et al., 1979). It was expected that responses of striate cells submissively reflected the sum of excitatory inputs from geniculate cells when intra-cortical inhibitions were excluded. During the bicuculline application, different interactions between the subareas were observed in the two groups of simple ceils. Receptive fields of striate cells were mapped with a stationary slit while bicuculline was withheld with negative currents (IS-20 nA). Thirty-two cells were classified as simple cells. The bicuculline application with positive currents (30-150 nA) successfully reduced the orientation selectivity in 25 of the 32 cells. The criterion was that the peak amplitude of their responses to a stationary long (> 5’) slit with an orientation orthogonal to the optimal become more than 50% of that to a slit with the optimal orientation. Accompanying this reduction of the orientation selectivity. the antagonism between the subareas diminished. Although no responses were evoked in normal condition by the stimuli which covered the whole receptive fields [Figs 7(F) and S(F). the bicuculline application released excitatory responses to the stimuli. On-off responses were evoked in the simple cells with two or three subareas [20 cells, Fig. 7(l)], while either on or off responses were evoked in the simple cells which showed one subarea to a single small slit [5 cells, Fig. 8(I)]. The sign of the responses evoked in the latter cells was the same as that of their responses in the central area. The manner in which the simple cell illustrated in Fig. 8 responded to the three kinds of stimuli during the bicuculline application is similar to that of oncenter geniculate cells. On-center geniculate cells show on discharges to a stimulus covering the center area of their receptive fields and off discharges to a stimulus coverging their surround fields, while weaker on discharges are displayed to a stimulus covering the whole part of their receptive fields (Hubel and Wiesel, 1961). Therefore, it is very likely that the simple cell received excitatory inputs exclusively from on-center geniculate cells. The off discharges evoked in its surround field might have their source in the surround excitations of the on-center geniculate inputs. If these off responses had come from off-center geniculate inputs, off discharges in
addition to on discharges should been evoked in the simple cell by the stimulus covering the whole receptive field [Fig. S(I)]. On the other hand. the on-off responses in the remaining simple cells to the stimulus covering the whole receptive field [Fig. 7(I)] suggest that these cells recieved converging on-center and off-center geniculate inputs. Although both center and surround excitations are displayed in Y geniculate cells to the diffuse light flashing (Tanaka. l983a), the surround excitations become negligible as the stimulus size decreases. The stimuli used in the present study to cover the whole receptive field of the simple cells were relatively small (2-3’ in size). Stimuli of such a size never evoked on-off discharges in Y geniculate cells (own observation). Moreover, these simple cells showed on-off discharges even to smaller stimuli located at the border between their subareas. It is improbable, therefore, that the on-off discharges of the simple cells came from on-off discharges of either on-center or off-center Y geniculate cells. DISCUSSION
The present study shows that lateral geniculate cells exert monosynaptic excitations on complex striate cells as well as on simple striate cells. These connections are functionally significant; the geniculate excitations contribute to discharges of striate cells in response to photic stimuli. The study further points out that the parallel channels in the lateral geniculate nucleus, i.e. X and Y cells or on-center and off-center cells are mixed in many individual striate cells. The striate cells can be divided into several groups depending on whether they receive mixed inputs or pure inputs, and on whether the mixed inputs are spatially overlapping or separated. The contribution of single geniculate inputs to responses of a striate cell was calculated during stimulation with a moving light slit. The values were smaller for complex cells (mean, 0.03) than for simple cells (mean, 0. I), which suggests that more geniculate cells converge to a complex cell than to a simple cell. However, a possibility that complex cells receive excitations from other cortical cells as well as from geniculate cells, is not denied in the present study. If the cortical excitatory inputs to complex cells are significantly strong, the convergence number of geniculate cells onto a complex cell may be smaller. The balance between geniculate excitations and cortical excitations in complex cells should be examined in the future. The convergence of 2-5 geniculate cells was actually demonstrated in I7 striate cells. The number of geniculate inputs revealed was relatively small when compared to those expected from the values of the contribution. This is natural in that only a limited number (3-19) of geniculate cells were sampled in pair with each of the striate cells. Because a significant portion of geniculate inputs to individual striate cells might be missed, even if only on-center or off-center
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of genicuiostriate
inputs, or X or Y inputs were exclusively revealed in a striate cell, it is not possible to conclude that the striate cell receive pure converging inputs from these kinds of geniculate cells. The on-off convergence was actually demonstrated in one simple cell. The responses of simple cells during the bicuculline application suggest that this is commonly true for a major subgroup of simple cells. The remaining simple ceils receive pure on-center or pure off-center inputs. The latter cells might be viewed as simple cells in some of the previous studies (Hubel and Wiesel, 1959; Gilbert, 1977), while they might be distinguished as a unique class of striate cells in other studies (Toyama and Takeda. 1974; Toyama et ul.. 1981). The on-OK convergence was also revealed in major complex cells. The on inputs and off inputs to complex cells are spatially overlapping. while those to simple cells are separated. The convergence of X and Y geniculate inputs could be expected for single simple cells and single standard-complex cells, since it was found that both groups of striate cells, as each cell group, receive excitations from both X and Y cells. Special-complex cells may receive Y inputs exclusively. The X-Y was actually demonstrated in 3 convergence standard-complex cells and 1 simple cell. A previous study examined responses of simple cells during the bicuculline application in connection with a set of photic stimuli which differentiated excitations in X and Y geniculate cells, and indicated that most simple cells receive pure X inputs or pure Y inputs (Tanaka, 1983a). Therefore, the X-Y convergence may occur mainly in standard-complex cells. As illustrated in Fig. 9, the present study suggests that there are several parallel channels in the cat striate cortex. Cells in the different channels receive geniculate excitations in different ways. REFERENCES Bullier J. and Henry G. neurons in cat striate 1751-1263.
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335-398. Hubel D. H. and W~rscl T. S. (lY61) Rcceptivc licldb. binocular interaction and functional architecture in the cat’s wual cortex. J. Ph~sioi.. Loncl. 160, 106-l 5-l Movshon J. ;\. (1975) The velocity tuning of single units in cat striate cortex. J. PI~,rsio/.. Land 249, -I-l5~6S. Sillito A. M. (1975) The effectiveness of bicuculline as an antagonist of GABA and visually evoked inhibition in the Cal’s striate cortex. J. PIf~sio~.. Lonrl. 250, 287-304 Mlito A. M. (1975) The contribution of inhibitory mcchanisms to the receptive field properties of neurones in the striate cortex of the cat. J. Ph~siol.. Loncl. 250, 305 329. Singer W.. Tretter F. and Cyander M. (1975) Oreanization of cat striate cortex: a correlation of receptive-geld properties with afferent and etrerent connections. J. .Vwrnplt~siol. 38, lOSo-- 1098. Stone J. and Dreher B. (IY73) Projection of X- and Y-cells of the cat’s lateral grniculate nucleus to areas I7 and I8 of visual c0rte.x. J. :\‘cwqd~~~.~io/.36, 551-567 Tanaka K. (1983) Distinct X- and Y-streams in the cat wsuul cortex revealed by bicuculline application. Rrczin Res. 265, 143-337. Tanaka K. (IYY3) Cross-correlation analysis of gcmcuiostriate neuronal relationships in cats. J. .Vrrtr~&~siol. 49, 1303-1318. Toyama K., Maekabva K. and Takeda T. (1973) An analysis of neuronal circuitry for two types of visual cortical neurones classified on the basis of their responses to photic stimuli. Brain Res. 61, 395-399. Toyama K.. Matsunami K.. Ohno T. and Tokashikl S. (1974) An intracellular study of neuronal organization in the Lisual cortex. Espl Brain Res. 21, 4566. Toyama K. and Takeda T. (1974) A unique class of cat‘s visual cortical cells that exhibit either ON or OFF excitation for stationary light slits and are responsive IO moving edge patterns. Bruin Res. 73, 35&355. Toyama K.. Kimura M. and Tanaka K. (I981 ) Crosscorrelation analysis of interneuronal connectivity in cat visual cortex. J .~ewupl~~sio~. 46, l9l-101. Wilson P. D.. Rowe M. H. and Stone J. (1976) Properliec of relay cells in cat’s lateral geniculate nucleus: a comparison of W-cells with X- and Y-cells J .\;~rrrr~/~lr~.vic~/. 39. 1193-1209