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Direction asymmetry by moving stimuli and static receptive field plots for simple cells in cat striate cortex
Cop!nght
0042.6989 84 S3 00 - 0.00 IJ IYS4 Pergamon Press Lrd
DIRECTION ASYMMETRY BY MOVING STIMULI AND STATIC RECEPTIVE FIELD PLOTS FOR SIMPLE CELLS IN CAT STRIATE CORTEX P. HEGGELGKD Neurobiological
Laboratory.
University
of Trondheim.
N-7055
Dragvoll-Trondheim.
Norway
Abstract-It has been suggested that direction asymmetry of simple cells by moving stimuli is due to asymmetries in Hanking response regions in the receptive field, and that the stronger response in the preferred direction is caused by synchronized On- and Off-responses. The hypothesis was tested by comparing the response of direction asymmetric cells to moving and static stimuli. The hypothesis had a weak but statistically significant predictive power. However, both for cells where the predicted preferred direction was correct and where it was wrong, there was clear suppression of the response in the nonpreferred movement direction. indicating that direction asymmetry is due to inhibitory processes rather than to synchronized On and Off-responses. It is suggested that the asymmetries in flanking regions of static receptive field plots are caused by the same inhibition which produces direction asymmetry, thus explaining why the static plots have some predictive power on direction asymmetry.
Direction
asymmetry
Striate cortex
Receptive
INTRODUCTION
an optimally oriented slit or edge moves forward and backward across the receptive field, the majority of simple cells in cat striate cortex respond stronger in one of the two opposite directions (Hubel and Wiesel, 1959, 1962). For some of these direction asymmetric cells the preferred direction withstands a reversal of image contrast, and these cells are commonly called direction selective. Hubel and Wiesel (1959, 1962) found that the response of simple cells to moving stimuli could be predicted from a plot of the On- and Off-response regions. They ascribed the direction asymmetry to asymmetries in the Ranking regions of the statically plotted discharge field (DF), and suggested that the stronger response in the preferred direction is due to synchronized On- and Off-responses as a light slit leaves an Off-region and enters an On-zone. Henry and Bishop (1972) showed examples of cells where the direction asymmetry could not be explained this way, and pointed out that the hypothesis fails to account for cells which lack response in the nonpreferred direction, and for the direction selective cells which do not reverse direction preference by contrast reversal. Several lines of evidence indicate that the direction asymmetry is produced primarily by inhibition acting in the nonpreferred direction (Benevento er al.. 1972; Henry and Bishop, 1972; lnnocenti and Fiore, 1974; Goodwin et al., 1975; Emerson and Gerstein, 1977; Sillito, 1977; Tsumoto et a/., 1979). Emerson and Gerstein (1977) found evidence for three different mechanisms: superposition of On- and Off-responses, forward inhibition in the nonpreferred direction, and forward facilitation in the preferred direction. Palmer and Davis (1981) compared responses to static stimuli with responses to moving stimuli and showed When
13
field
Simple cells
Cat
that responses to a light slit occurred where it entered an On-zone or left an Off-zone. For the majority of the cells they could explain the direction asymmetry by synchronized On- and Off-responses, although the response to moving stimuli usually deviated from strict superposition of On- and Off-responses. Previous papers where it has been reported that direction asymmetry can be predicted from static plots of On- and Off-regions, lack information on the proportion of cells where the prediction was successful. This is important since just by chance the predictions would be correct in 50% of the cases. The present investigation was made to study whether synchronized On- and Off-response actually contributes to formation of direction asymmetry. The results showed that the hypothesis had a weak but statistically significant predictive power. However, for almost all cells the results showed that the response was suppressed in the nonpreferred direction, indicating that the direction asymmetry was produced by inhibitory processes rather than by synchronized On- and Off-responses. \lETHODS
The general methods have been described in detail elsewhere (Heggelund, 1981). Single units in the striate cortex of adult cats were recorded with tungsten in glass microelectrodes (Levick, 1972) in long penetrations through the medial bank of the post-lateral gyrus near Horsley-Clarke coordinates posterior 3 mm, lateral 1.5 mm. The animals were anesthetized (pentobarbital) and immobilized (gallaminethriethiodide 6 mg/kg/hr). Bilateral section of the cervical sympathetic chain was made to minimize residual eye-movements. The On- and Off-responses to an optimally oriented light slit (0.15-0.3 deg wide) was determined
1-t
P. HEGGELLXV
in a series of broad-side positions across the discharge field (staric DP-ploll. The window time for the On- and the Off-periods were equal for each cell but varied between 0.5 and l.Osec from ceii to cell. The various receptive field positions were tested in an interleaved manner. and the number of repeated measurements in each position varied between IO and 30 from cell to cell. The luminance of the slit was luminance 0.3-1.0 log unit above background (2.4 cd’m’). For each ceil the response to an optimally oriented light slit which moved forward and backward across the receptive field was also determined. The slit had the same dimensions and luminance as the stimulus used for the static DF-plot. Slow angular velocities in she range 0.5-~Odeg~sec were used. The number of sweeps varied between 10 and 30 from cell to cell. The direction asymmetry to the moving slit was defined by the following index: DA = (PD - NPD)/PD, where PD is the peak firing rate to the slit moving in the preferred direction, and NPD the peak firing rate in the nonpreferred direction. Considering the response variability of the cells (Heggelund and Albus, 1978), direction asymmetries above 0.2 were considered to be significantly different from zero. This is a lower criterion for direction asymmetry than used in several previous studies (e.g. Albus, 1980; Orban et al., 1981), and it was chosen to include cells with moderate direction asymmetry where synchronization of On- and Off-responses might be important for the formation of the direction asymmetry. RESULTS
Data were analyzed for 73 simple cells which had their receptive field centered within 6deg from area centralis. Sixty-one of the cells (84%) had direction asymmetries above 0.2, and the analyses below were based on these cells. The plots of the On- and Off-responses across the receptive field showed a large variety of distributions (Hubel and Wiesel, 1962). The cells were subdivided into On- and Off-dominant depending on which response was strongest (Heggelund, 1981). Some Ondominant cells had weaker Off-response on both sides of the dominant On-zone, but the OR-response was always stronger on one side (Fig. 1). Other Ondominant cells had Off-response almost only on one side (Fig. 3). Corresponding configurations were found among the Off-dominant cells (Figs 2 and 4). When the responses to the ,noving slit were compared to the static DF-plot, the responses occurred typically where the slit entered an On-zone or left an Of&zone (Figs l-4) in accordance with the findings of Palmer and Davis ( I!% i ). According to the hypothesis that direction asymmetry is produced by synchronized On- and Offresponses, On-dominant simple cells should prefer movement into the On-zone from the Rank where the
178 i -3
0
---
3
Distance from 9F idcg ) Fig. I. Comparison of responsesIO a stationary flashing and a moving optimally oriented light slit (0.17 x 3.3 deg) for an On-dominant simple cell. By the static DF-plot (upper figure) the slit was presented On and OIT’ in broadside positions across the discharge field (DF). The abscissa shows the broadside distances from the DF-center as determined by hand-plotting. In each position 16 On- and OIT-presentations were made. The ordinate shows mean peak firing rate during the On- respective OQeriods. The window time for both periods were 0.5 sec. The lower figure shows a perisrimulus time histogram (PSTH) for the response to 16 sweeps of the slit across the receptive field from the minus to the plus side. and back. The slit moved across the 6deg in each direction in 2sec (3deg/sec). The same abscissa as by the static DF-plot was used, and the ordinate shows mean firing rates.
strongest Off-response occurs (from the plus to the minus side in Fig. I). Off-dominant cells should prefer movement out from the Off-zone to the flank where the strongest On-response occurs (from the minus to the plus side in Fig. 3). These predictions were correct for 40 of the 61 direction asymmetric cells (66%). Although this was only 16% above the chance level, the predictions were significantly better than chance (P c 0.01). For almost all cells where these predictions were correct it was clear that the direction asymmetry was not produced by synchronized On- and Off-response, but mainly by suppression in the nonpreferred movement direction as illustrated for an Ondominant cell in Fig. 1. To simplify comparison ot the response lo the static and the moving stimulus the results for both conditions were plotted on the same abscissa. When the slit moved across the DF in the nonpreferred direction (from the minus to the plus side) there was first a synchronized Off- and Onresponse as the slit left the Off-zone on the minus side and entered the dominant On-region, and then a second very weak response as the slit moved out from the Off-region on the plus side. In the preferred direction
also two responses occurred:
synchronized
Off- and On-response
the first was ;!
from leaving the
Direction
asymmetry
by moving
stimuli
DC
S:ctlC
75[,N
E
Sfaflc
i
62
Moving
DF
Sllf
5
0
-:c. 62 1 r
r
-3
0 Distance
from
DF Ideg
Off-zone on the plus side and entering the dominant On-region. the second occurred as the slit left the Offzone on the minus side. Although the Off-zone on the minus side was the least responsive one in the static DF-plot, the response by leaving this zone in the preferred direction was much stronger than the response by leaving the Off-zone on the plus side in the nonpreferred direction. In fact, the response by leaving the Off-region on the minus side in the preferred direction was almost as strong as the synchronized Off- and On-response in the nonpreferred direction. This rather weak response in the nonpreferred direction compared with the brisk Onresponse by the static DF-plot shows that the response was strongly suppressed in the nonpreferred direction. Results from an Off-dominant cell which had the most responsive On-zone on the plus side, is shown in Fig. 2. By slit movement in the preferred direction the cell first responded as the slit entered the On-zone on the minus side, and then gave a strong synchroneous Off- and On-response upon leaving the dominant region and entering the most responsive On-zone. In the nonpreferred direction the cell gave a weak response as the slit passed the most responsive On-zone, and then an even weaker synchroneous Offand On-response as the slit left the dominant Offzone and entered the On-zone on the minus side. By comparing the weak response in the nonpreferred direction with the strong responses in the static DFplot it is clear that the response was markedly suppressed when the slit moved in the nonpreferred direction.
0 Orstance
I
Fig. 2. Results from an Off-dominant simple cell obtained with an optimally oriented light slit (0.15 x 3.8 deg). The On- and OK-periods in the static DF-plot were 0.5 sec. and the plot is based on IO presentations in each position. By the PSTH to the moving stimulus the slit crossed the 6deg in each direction in 3 set (2deg;sec). Ten sweeps were made.
I
-3
3
3
from DF (deg)
Results from an On-dominant simple cell obtained with an optimally oriented light slit (0.2 x 3.1 deg). The window times by the static DF-plot was OSsec, and IO presentations in each position were made. By the moving stimulus the slit swept across the 6deg in each direction in 6 set (I de.g,‘sec). Ten sweeps were made. Fig.
3.
For the cells where the prediction of preferred direction was correct there was no clear relationship between degree of flank asymmetry in the static DF-plot and the degree of direction asymmetry. The On-dominant cell from Fig. I. e.g. had only slightly stronger Off-response on the plus than on the minus side, but still it had marked direction asymmetry (0.8). The On-dominant simple cell illustrated in Fig. 3 had Off-response almost only on the one side but still the degree of direction asymmetry was moderate (0.4). Also for the cells where the preferred direction predicted from the static DF-plot was wrong, the direction asymmetry was mainly produced by suppression in the nonpreferred direction as illustrated by Fig. 4. This Off-dominant cell had an On-region only on the plus side, but still it preferred slit movement from the plus to the minus side. As one would expect from the static DF-plot the cell gave a synchronized Off- and On-response as the slit moved out from the Off-zone and into the On-region (nonpreferred direction). But this synchronized Offand On-response was weak compared to the two responses elicited by the slit in the preferred direction upon entering the On-zone respective leaving the Offregion, and the results clearly show that the response was suppressed in the nonpreferred direction. DISCUSSION
The plots of On- and Off-responses across the receptive field had only weak predictive power for the direction asymmetry by moving light slits. Nevertheless, the predictive power was significantly better
P. HEGGELLND
excitatory With :he
and inhtbitor)
ticI&
such arrangement tUo
Hanks
position uould
bcsidc JitIPr.
the most and ,uch
explain direction asymmctr> the asymmetry static
would
13x1 I_
responsibc .t>;.n:rn~try
h! mo\ I”:
of the flankins
DF-plot
location
(tlcygciurtd.
the dcprer I\( inhibition
coti;J
sttmuli.
-\IsP
respon\c regions in the
be pxrrl!
of’ the eucitatorh
<‘II DF-
dct:rn:ined
field.
Thi,
bl
:hc
:tsymmetr*,
would vary wtth the reLttt\.c dtarncter of the tu\) tields, the distance betueen thetr ccntcr5. and wtth the \veight of Inhibition lund.
‘---I--t
180 1
I -3 Distance
0 from OF
3
(deg)
Fig. 4. Off-dominant simple cell tested with a 0.18 x 2.9deg light slit. The window times by the static DF-plot were 0.5~~. and IO measurements were made in each position. The moving slit crossed the 6 deg tn each direction in 2 set (3deg/sec). and the plot was based on IO sweeps.
than chance indicating that there is some correlation
between the spatial distribution of On- and Offresponses, and direction asymmetry. This low predictive power indicates that synchronized On- and Off-responses hardly plays any important role for formation of direction asymmetry. Furthermore, both for the cells where the preferred direction predicted from the static DF-plot was correct and where it was wrong, the results showed that direction asymmetry was mainly produced by suppression in the nonpreferred direction. This is consistent with the hypothesis that direction asymmetry is due to inhibition acting in the nonpreferred direction. and this hypothesis is supported by several lines of evidence. Data obtained with intracellular recording techniques have strongly indicated that direction asymmetry derives from intracortical post-synaptic inhibitory input (Benevento ef al., 1972; Innocenti and Fiore, 1974), and this is further supported by the finding that direction asymmetry is reduced or abolished by blockage of GABAmediated intracortical inhibition (Sillito, 1977; Tsumoto et al., 1979). Goodwin et al. (1975) showed that direction asymmetry is produced by suppression spreading out in front of the stimulus in the nonpreferred direction. Also from the results of Emerson and Gerstein (1977) where three different mechanisms for direction asymmetry were found, it appears that suppression in the nonpreferred direction has a more basic character than the other two mechanisms; such suppression was found in all the cells they tested whereas superposition of On- and Off-responses and facilitation in the preferred direction occurred only by some cells. The receptive field organization of simple cells can be explained by partly overlapping but acentric
1981).
asymmetry
The
rclattii‘
to c\c:tztton
direction
of Hank response
nsymrnetr~
\rould
explain
uhy
the
in the static DF-plot
could thus be due to the same inhibitory and this
(Fieggcand
static
processes.
DF-plots
have
some predictive power on direction aqmmetrq. .-l~X,,o,~Ic~(clc~,,rc,nrv----I wish
IO
thank
\‘er;t
SchulT
for
technical assistance. nnd Dr Johannes Moors who participated m some experiments at an early st‘tge of the project. The work was supported by the Norwegian Council for Scienceand the Humanities
Research
REFERENCES Albus I(. (1980) The detection of movement direction and effects of contrast reversal in the cat‘s striate cortex. l’i.rion Rex. 20, 289-293. Benevento L. A., Creutzfcldt 0. !) -nii Kuhnt U. Significance of intracortical inhibition in the visual cortex. Nnrttre. New Biol. 238, 125-l 26. Emerson R. C. and Gerstein G L. (19771 Simple striate neurons in the cat. II. Mechanisms underlying direction asymmetry and direction selectivity. .I \‘c!rrop/rJ~.rio/ 40, 136-155. Goodwin A. W., Henry G. ll ;ind B~\!lop I’. 0. (1975) Direction selectivity of simple striate cells: Properties and mechanisms. J. Neuroph~uiol. 38, I NO- 1523. Heggelund P. (1981) Receptive field orgamzation of simple cells in cat striate cortex. E~pl Rroin Rcs 42, 89-98. Heggelund P. and Albus K. (1978) Response variability and orientation discrimination of single cells in striate cortex uf cat. Espl Brain Res. 32. 197--21 I. Henry G. H. and Bishop P 0 11973) Striate neuroncs receptive field organization. //II (‘31 Ophrlinl. I I, 357-368 Hubel D. H. and Wiescl T U (1959) Receotivc fields ot single neurones in the cdl’> \triatc cortex J. Ph.wo/. Land. l48,574-59 1. Hubel D. H. and Wiesel ‘I \ ti9611 Receptive fields. binocular interaction. and functional Jrchitecture in the cat’s visual cortex. J. Ph.wol.. Lund 160. 106-154 Innocenti G. M. and Fiorc L (197-i) Post-synaptic inhibitory components of the response< to moving stimuli in area 17. Brain REF. 80. IX- I26 Levick W. R. (1972) Another tungsten microelectrode Med. Viol. Eng. Compur. 10, 5l(tSl>. Orban G. A.. Kennedv H. and Maes H. (1981) Response to movement of neurons in areas 17 and I8 of ‘the cat’ Direction selectivity. J. .Veurophxrlo/. 45, 1059-1073. Palmer L. A. and Davis T. L. (1981) Comparison 01 responses to moving and stationary stimuli in cat striate cortex. J. Neurophysiol. 44. 277-295. Sillito A. M. (1977) Inhibitory processes underlying the direction specifcity simple.complex dnd hypercomplrx cells in the cat’s visual cortex. J. Ph~siol.. Land. 271, 699-720. Tsumoto T., Eckart W. and Creutzfeidt 0 D. (1979) Modification of orientation sensitivity of visual cortex neurons by removal of GABA-mediated inhibition E.rpl Brain Res. 31, 351-363
of
0042.6989 84 S3 00 - 0.00 IJ IYS4 Pergamon Press Lrd
DIRECTION ASYMMETRY BY MOVING STIMULI AND STATIC RECEPTIVE FIELD PLOTS FOR SIMPLE CELLS IN CAT STRIATE CORTEX P. HEGGELGKD Neurobiological
Laboratory.
University
of Trondheim.
N-7055
Dragvoll-Trondheim.
Norway
Abstract-It has been suggested that direction asymmetry of simple cells by moving stimuli is due to asymmetries in Hanking response regions in the receptive field, and that the stronger response in the preferred direction is caused by synchronized On- and Off-responses. The hypothesis was tested by comparing the response of direction asymmetric cells to moving and static stimuli. The hypothesis had a weak but statistically significant predictive power. However, both for cells where the predicted preferred direction was correct and where it was wrong, there was clear suppression of the response in the nonpreferred movement direction. indicating that direction asymmetry is due to inhibitory processes rather than to synchronized On and Off-responses. It is suggested that the asymmetries in flanking regions of static receptive field plots are caused by the same inhibition which produces direction asymmetry, thus explaining why the static plots have some predictive power on direction asymmetry.
Direction
asymmetry
Striate cortex
Receptive
INTRODUCTION
an optimally oriented slit or edge moves forward and backward across the receptive field, the majority of simple cells in cat striate cortex respond stronger in one of the two opposite directions (Hubel and Wiesel, 1959, 1962). For some of these direction asymmetric cells the preferred direction withstands a reversal of image contrast, and these cells are commonly called direction selective. Hubel and Wiesel (1959, 1962) found that the response of simple cells to moving stimuli could be predicted from a plot of the On- and Off-response regions. They ascribed the direction asymmetry to asymmetries in the Ranking regions of the statically plotted discharge field (DF), and suggested that the stronger response in the preferred direction is due to synchronized On- and Off-responses as a light slit leaves an Off-region and enters an On-zone. Henry and Bishop (1972) showed examples of cells where the direction asymmetry could not be explained this way, and pointed out that the hypothesis fails to account for cells which lack response in the nonpreferred direction, and for the direction selective cells which do not reverse direction preference by contrast reversal. Several lines of evidence indicate that the direction asymmetry is produced primarily by inhibition acting in the nonpreferred direction (Benevento er al.. 1972; Henry and Bishop, 1972; lnnocenti and Fiore, 1974; Goodwin et al., 1975; Emerson and Gerstein, 1977; Sillito, 1977; Tsumoto et a/., 1979). Emerson and Gerstein (1977) found evidence for three different mechanisms: superposition of On- and Off-responses, forward inhibition in the nonpreferred direction, and forward facilitation in the preferred direction. Palmer and Davis (1981) compared responses to static stimuli with responses to moving stimuli and showed When
13
field
Simple cells
Cat
that responses to a light slit occurred where it entered an On-zone or left an Off-zone. For the majority of the cells they could explain the direction asymmetry by synchronized On- and Off-responses, although the response to moving stimuli usually deviated from strict superposition of On- and Off-responses. Previous papers where it has been reported that direction asymmetry can be predicted from static plots of On- and Off-regions, lack information on the proportion of cells where the prediction was successful. This is important since just by chance the predictions would be correct in 50% of the cases. The present investigation was made to study whether synchronized On- and Off-response actually contributes to formation of direction asymmetry. The results showed that the hypothesis had a weak but statistically significant predictive power. However, for almost all cells the results showed that the response was suppressed in the nonpreferred direction, indicating that the direction asymmetry was produced by inhibitory processes rather than by synchronized On- and Off-responses. \lETHODS
The general methods have been described in detail elsewhere (Heggelund, 1981). Single units in the striate cortex of adult cats were recorded with tungsten in glass microelectrodes (Levick, 1972) in long penetrations through the medial bank of the post-lateral gyrus near Horsley-Clarke coordinates posterior 3 mm, lateral 1.5 mm. The animals were anesthetized (pentobarbital) and immobilized (gallaminethriethiodide 6 mg/kg/hr). Bilateral section of the cervical sympathetic chain was made to minimize residual eye-movements. The On- and Off-responses to an optimally oriented light slit (0.15-0.3 deg wide) was determined
1-t
P. HEGGELLXV
in a series of broad-side positions across the discharge field (staric DP-ploll. The window time for the On- and the Off-periods were equal for each cell but varied between 0.5 and l.Osec from ceii to cell. The various receptive field positions were tested in an interleaved manner. and the number of repeated measurements in each position varied between IO and 30 from cell to cell. The luminance of the slit was luminance 0.3-1.0 log unit above background (2.4 cd’m’). For each ceil the response to an optimally oriented light slit which moved forward and backward across the receptive field was also determined. The slit had the same dimensions and luminance as the stimulus used for the static DF-plot. Slow angular velocities in she range 0.5-~Odeg~sec were used. The number of sweeps varied between 10 and 30 from cell to cell. The direction asymmetry to the moving slit was defined by the following index: DA = (PD - NPD)/PD, where PD is the peak firing rate to the slit moving in the preferred direction, and NPD the peak firing rate in the nonpreferred direction. Considering the response variability of the cells (Heggelund and Albus, 1978), direction asymmetries above 0.2 were considered to be significantly different from zero. This is a lower criterion for direction asymmetry than used in several previous studies (e.g. Albus, 1980; Orban et al., 1981), and it was chosen to include cells with moderate direction asymmetry where synchronization of On- and Off-responses might be important for the formation of the direction asymmetry. RESULTS
Data were analyzed for 73 simple cells which had their receptive field centered within 6deg from area centralis. Sixty-one of the cells (84%) had direction asymmetries above 0.2, and the analyses below were based on these cells. The plots of the On- and Off-responses across the receptive field showed a large variety of distributions (Hubel and Wiesel, 1962). The cells were subdivided into On- and Off-dominant depending on which response was strongest (Heggelund, 1981). Some Ondominant cells had weaker Off-response on both sides of the dominant On-zone, but the OR-response was always stronger on one side (Fig. 1). Other Ondominant cells had Off-response almost only on one side (Fig. 3). Corresponding configurations were found among the Off-dominant cells (Figs 2 and 4). When the responses to the ,noving slit were compared to the static DF-plot, the responses occurred typically where the slit entered an On-zone or left an Of&zone (Figs l-4) in accordance with the findings of Palmer and Davis ( I!% i ). According to the hypothesis that direction asymmetry is produced by synchronized On- and Offresponses, On-dominant simple cells should prefer movement into the On-zone from the Rank where the
178 i -3
0
---
3
Distance from 9F idcg ) Fig. I. Comparison of responsesIO a stationary flashing and a moving optimally oriented light slit (0.17 x 3.3 deg) for an On-dominant simple cell. By the static DF-plot (upper figure) the slit was presented On and OIT’ in broadside positions across the discharge field (DF). The abscissa shows the broadside distances from the DF-center as determined by hand-plotting. In each position 16 On- and OIT-presentations were made. The ordinate shows mean peak firing rate during the On- respective OQeriods. The window time for both periods were 0.5 sec. The lower figure shows a perisrimulus time histogram (PSTH) for the response to 16 sweeps of the slit across the receptive field from the minus to the plus side. and back. The slit moved across the 6deg in each direction in 2sec (3deg/sec). The same abscissa as by the static DF-plot was used, and the ordinate shows mean firing rates.
strongest Off-response occurs (from the plus to the minus side in Fig. I). Off-dominant cells should prefer movement out from the Off-zone to the flank where the strongest On-response occurs (from the minus to the plus side in Fig. 3). These predictions were correct for 40 of the 61 direction asymmetric cells (66%). Although this was only 16% above the chance level, the predictions were significantly better than chance (P c 0.01). For almost all cells where these predictions were correct it was clear that the direction asymmetry was not produced by synchronized On- and Off-response, but mainly by suppression in the nonpreferred movement direction as illustrated for an Ondominant cell in Fig. 1. To simplify comparison ot the response lo the static and the moving stimulus the results for both conditions were plotted on the same abscissa. When the slit moved across the DF in the nonpreferred direction (from the minus to the plus side) there was first a synchronized Off- and Onresponse as the slit left the Off-zone on the minus side and entered the dominant On-region, and then a second very weak response as the slit moved out from the Off-region on the plus side. In the preferred direction
also two responses occurred:
synchronized
Off- and On-response
the first was ;!
from leaving the
Direction
asymmetry
by moving
stimuli
DC
S:ctlC
75[,N
E
Sfaflc
i
62
Moving
DF
Sllf
5
0
-:c. 62 1 r
r
-3
0 Distance
from
DF Ideg
Off-zone on the plus side and entering the dominant On-region. the second occurred as the slit left the Offzone on the minus side. Although the Off-zone on the minus side was the least responsive one in the static DF-plot, the response by leaving this zone in the preferred direction was much stronger than the response by leaving the Off-zone on the plus side in the nonpreferred direction. In fact, the response by leaving the Off-region on the minus side in the preferred direction was almost as strong as the synchronized Off- and On-response in the nonpreferred direction. This rather weak response in the nonpreferred direction compared with the brisk Onresponse by the static DF-plot shows that the response was strongly suppressed in the nonpreferred direction. Results from an Off-dominant cell which had the most responsive On-zone on the plus side, is shown in Fig. 2. By slit movement in the preferred direction the cell first responded as the slit entered the On-zone on the minus side, and then gave a strong synchroneous Off- and On-response upon leaving the dominant region and entering the most responsive On-zone. In the nonpreferred direction the cell gave a weak response as the slit passed the most responsive On-zone, and then an even weaker synchroneous Offand On-response as the slit left the dominant Offzone and entered the On-zone on the minus side. By comparing the weak response in the nonpreferred direction with the strong responses in the static DFplot it is clear that the response was markedly suppressed when the slit moved in the nonpreferred direction.
0 Orstance
I
Fig. 2. Results from an Off-dominant simple cell obtained with an optimally oriented light slit (0.15 x 3.8 deg). The On- and OK-periods in the static DF-plot were 0.5 sec. and the plot is based on IO presentations in each position. By the PSTH to the moving stimulus the slit crossed the 6deg in each direction in 3 set (2deg;sec). Ten sweeps were made.
I
-3
3
3
from DF (deg)
Results from an On-dominant simple cell obtained with an optimally oriented light slit (0.2 x 3.1 deg). The window times by the static DF-plot was OSsec, and IO presentations in each position were made. By the moving stimulus the slit swept across the 6deg in each direction in 6 set (I de.g,‘sec). Ten sweeps were made. Fig.
3.
For the cells where the prediction of preferred direction was correct there was no clear relationship between degree of flank asymmetry in the static DF-plot and the degree of direction asymmetry. The On-dominant cell from Fig. I. e.g. had only slightly stronger Off-response on the plus than on the minus side, but still it had marked direction asymmetry (0.8). The On-dominant simple cell illustrated in Fig. 3 had Off-response almost only on the one side but still the degree of direction asymmetry was moderate (0.4). Also for the cells where the preferred direction predicted from the static DF-plot was wrong, the direction asymmetry was mainly produced by suppression in the nonpreferred direction as illustrated by Fig. 4. This Off-dominant cell had an On-region only on the plus side, but still it preferred slit movement from the plus to the minus side. As one would expect from the static DF-plot the cell gave a synchronized Off- and On-response as the slit moved out from the Off-zone and into the On-region (nonpreferred direction). But this synchronized Offand On-response was weak compared to the two responses elicited by the slit in the preferred direction upon entering the On-zone respective leaving the Offregion, and the results clearly show that the response was suppressed in the nonpreferred direction. DISCUSSION
The plots of On- and Off-responses across the receptive field had only weak predictive power for the direction asymmetry by moving light slits. Nevertheless, the predictive power was significantly better
P. HEGGELLND
excitatory With :he
and inhtbitor)
ticI&
such arrangement tUo
Hanks
position uould
bcsidc JitIPr.
the most and ,uch
explain direction asymmctr> the asymmetry static
would
13x1 I_
responsibc .t>;.n:rn~try
h! mo\ I”:
of the flankins
DF-plot
location
(tlcygciurtd.
the dcprer I\( inhibition
coti;J
sttmuli.
-\IsP
respon\c regions in the
be pxrrl!
of’ the eucitatorh
<‘II DF-
dct:rn:ined
field.
Thi,
bl
:hc
:tsymmetr*,
would vary wtth the reLttt\.c dtarncter of the tu\) tields, the distance betueen thetr ccntcr5. and wtth the \veight of Inhibition lund.
‘---I--t
180 1
I -3 Distance
0 from OF
3
(deg)
Fig. 4. Off-dominant simple cell tested with a 0.18 x 2.9deg light slit. The window times by the static DF-plot were 0.5~~. and IO measurements were made in each position. The moving slit crossed the 6 deg tn each direction in 2 set (3deg/sec). and the plot was based on IO sweeps.
than chance indicating that there is some correlation
between the spatial distribution of On- and Offresponses, and direction asymmetry. This low predictive power indicates that synchronized On- and Off-responses hardly plays any important role for formation of direction asymmetry. Furthermore, both for the cells where the preferred direction predicted from the static DF-plot was correct and where it was wrong, the results showed that direction asymmetry was mainly produced by suppression in the nonpreferred direction. This is consistent with the hypothesis that direction asymmetry is due to inhibition acting in the nonpreferred direction. and this hypothesis is supported by several lines of evidence. Data obtained with intracellular recording techniques have strongly indicated that direction asymmetry derives from intracortical post-synaptic inhibitory input (Benevento ef al., 1972; Innocenti and Fiore, 1974), and this is further supported by the finding that direction asymmetry is reduced or abolished by blockage of GABAmediated intracortical inhibition (Sillito, 1977; Tsumoto et al., 1979). Goodwin et al. (1975) showed that direction asymmetry is produced by suppression spreading out in front of the stimulus in the nonpreferred direction. Also from the results of Emerson and Gerstein (1977) where three different mechanisms for direction asymmetry were found, it appears that suppression in the nonpreferred direction has a more basic character than the other two mechanisms; such suppression was found in all the cells they tested whereas superposition of On- and Off-responses and facilitation in the preferred direction occurred only by some cells. The receptive field organization of simple cells can be explained by partly overlapping but acentric
1981).
asymmetry
The
rclattii‘
to c\c:tztton
direction
of Hank response
nsymrnetr~
\rould
explain
uhy
the
in the static DF-plot
could thus be due to the same inhibitory and this
(Fieggcand
static
processes.
DF-plots
have
some predictive power on direction aqmmetrq. .-l~X,,o,~Ic~(clc~,,rc,nrv----I wish
IO
thank
\‘er;t
SchulT
for
technical assistance. nnd Dr Johannes Moors who participated m some experiments at an early st‘tge of the project. The work was supported by the Norwegian Council for Scienceand the Humanities
Research
REFERENCES Albus I(. (1980) The detection of movement direction and effects of contrast reversal in the cat‘s striate cortex. l’i.rion Rex. 20, 289-293. Benevento L. A., Creutzfcldt 0. !) -nii Kuhnt U. Significance of intracortical inhibition in the visual cortex. Nnrttre. New Biol. 238, 125-l 26. Emerson R. C. and Gerstein G L. (19771 Simple striate neurons in the cat. II. Mechanisms underlying direction asymmetry and direction selectivity. .I \‘c!rrop/rJ~.rio/ 40, 136-155. Goodwin A. W., Henry G. ll ;ind B~\!lop I’. 0. (1975) Direction selectivity of simple striate cells: Properties and mechanisms. J. Neuroph~uiol. 38, I NO- 1523. Heggelund P. (1981) Receptive field orgamzation of simple cells in cat striate cortex. E~pl Rroin Rcs 42, 89-98. Heggelund P. and Albus K. (1978) Response variability and orientation discrimination of single cells in striate cortex uf cat. Espl Brain Res. 32. 197--21 I. Henry G. H. and Bishop P 0 11973) Striate neuroncs receptive field organization. //II (‘31 Ophrlinl. I I, 357-368 Hubel D. H. and Wiescl T U (1959) Receotivc fields ot single neurones in the cdl’> \triatc cortex J. Ph.wo/. Land. l48,574-59 1. Hubel D. H. and Wiesel ‘I \ ti9611 Receptive fields. binocular interaction. and functional Jrchitecture in the cat’s visual cortex. J. Ph.wol.. Lund 160. 106-154 Innocenti G. M. and Fiorc L (197-i) Post-synaptic inhibitory components of the response< to moving stimuli in area 17. Brain REF. 80. IX- I26 Levick W. R. (1972) Another tungsten microelectrode Med. Viol. Eng. Compur. 10, 5l(tSl>. Orban G. A.. Kennedv H. and Maes H. (1981) Response to movement of neurons in areas 17 and I8 of ‘the cat’ Direction selectivity. J. .Veurophxrlo/. 45, 1059-1073. Palmer L. A. and Davis T. L. (1981) Comparison 01 responses to moving and stationary stimuli in cat striate cortex. J. Neurophysiol. 44. 277-295. Sillito A. M. (1977) Inhibitory processes underlying the direction specifcity simple.complex dnd hypercomplrx cells in the cat’s visual cortex. J. Ph~siol.. Land. 271, 699-720. Tsumoto T., Eckart W. and Creutzfeidt 0 D. (1979) Modification of orientation sensitivity of visual cortex neurons by removal of GABA-mediated inhibition E.rpl Brain Res. 31, 351-363
of