Neuroscience Vol. 18, No. 1, pp. 25 30, 1986 Printed in Great Britain

0306-4522/86 $3.00 + 0.00 Pergamon Press Ltd

© 1986 IBRO

INFLUENCE OF STIMULUS LENGTH ON DIRECTIONAL BIAS OF COMPLEX CELLS IN CAT STRIATE CORTEX

P. HAMMOND and G. S. V. MOUAT Department of" Communication and Neuroscience, University of Keele, Keele, Staffordshire ST5 5BG,

U.K.

Abstract--Visual cortical cells respond optimally to an oriented bar moving either in one unique direction or in directions 180 ° apart. Length-dependence of this direction selectivity was investigated in the striate cortex of lightly anaesthetized cats. Approaching half of all complex cells showed some lability in their direction selectivity. The incidence was highest in standard and intermediate (length-summating) complex cells, less amongst special complex cells (those with only localized summation) and least amongst end-stopped cells, especially those of the special category. By contrast, direction selectivity of simple cells was length-independent. No correlation between a cell's overt selectivity (i.e. bidirectional, direction- biased or direction-selective) and its lability with bar length or polarity of contrast (light/dark) was evident.

Moreover, since individual neurons amongst a population of complex cells could exhibit either increase, decrease, or no change of direction selectivity with length, it is unlikely that length per se can be coded by direction-selectivity.

Gilbert 4 segregated complex cells of the cat 's striate cortex into length-summating (standard) and non- length-summating (special) classes. Recently, we have re-examined this classificatory scheme and have had occasion to modify it. 2~8 We found that 39% of cells were special, responding optimally to contours of optimal orientation but much shorter than the min- imum response field estimate of receptive field length; 43% were standard, responding optimally to bars whose length equalled or exceeded the length of the minimum response field (by its nature, the minimum response field method significantly underestimates receptive field length). However, 18% of complex cells could not be typed in this way: they had length summation characteristics intermediate between those of special and standard complex cells; possibly they represent a continuum in the length summation do- main, but there is compelling evidence to suggest that they constitute a distinct third group of cells. Indeed, rigid application of the yardstick that the ratio of length summation to receptive field length must equal or exceed unity for standard complex cells raises the proport ion of these unclassifiable cells from 18% to as much as 34%.

Peterhans e t al. 2~ have recently described direction selectivity of simple cells in the cat 's striate cortex, applying a quantitative measure which compares the strength of response peaks in a cell's preferred and opposite directions:

(preferred - non-preferred)/preferred.

This measure has its merit but also its limitations because, expressed in this way, direction selectivities cannot exceed i00% -- i .e . no account is taken of resting discharge levels, or of null suppression whereby a stimulus moving in the direction opposite to that preferred by a cell may actually depress its firing below the resting level.

We have therefore adopted a slightly modified comparison, which takes account of these parameters and which we have applied primarily to complex cells. Thus, a cell's direction selectivity is defined by the ratio:

(preferred - non-preferred)/ (preferred - resting discharge).

[Note that it is not necessary to make allowance for resting discharge in the numerator, i.e.

(preferred - resting discharge) - (non -p re fe r r ed - resting discharge)

since the resting discharge terms cancel out.] The ratio is zero in bidirectional cells, between zero and unity in direction-biased cells; unity in direction- selective cells; and greater than unity in direction- selective cells exhibiting null-suppression. A reversal of preferred direction yields a negative ratio. In the course of the previously published measurements of complex cells' length summation, 2'8 we noted that the direction bias of a significant proport ion of cells varies with stimulus length. These results are reported here, together with data from a few simple cells for comparison.

E X P E R I M E N T A L P R O C E D U R E S

Recordings were made from lightly anaesthetized, para- lyzed, cats) ,6,~-~3 Except that animals recovered between periodic recording sessions, 5 these techniques were con- ventional. On a prior occasion, animals had been implanted under surgical anaesthesia with a closed chamber and a peg cemented to the skull for painless head restraint) After induction with nitrous oxide/oxygen/halothane (Fluothane, I.C.I.), animals were anaesthetized with 72.5%:27.5% ni- trous oxide:oxygen plus 0.25q).6% halothane during recording. Gallamine triethiodide (Flaxedil, May and Baker) was given intravenously; mydriasis (1% atropine sulphate; Minims, Smith and Nephew), retraction of nictitating mem- branes (10% phenylephrine hydrochloride; Minims, Smith

25

26 P. HAMMOND and G. S. V. MOUAT

and Nephew), corneal protection with unpowered contact lenses, 5 mm diameter artificial pupils and supplementary lenses ensured optical correction for a viewing distance of 57 cm. Artificial ventilation to 3.8-4.0% end-tidal carbon dioxide was maintained via a cuffed endotracheal tube. Carbon dioxide, electroencephalogram, electrocardiogram and heart rate, rectal temperature and neuronal firing rates were monitored throughout.

Four-M NaCl-filled micropipettes were used to isolate single cells. Vertical electrode tracks at precisely defined spacings were made on consecutive occasions through either cerebral hemisphere (3-6.5 mm behind the interaural plane, <2 mm from the midline). Thus, recordings were safely within area 17, from the lower contralateral quadrant of the visual field, within 9 ° of the area centralis.

Raw data were stored on tape cassettes. Waveform and polarity of neural impulses, and dot raster displays where each dot represented one impulse and each row one stimulus cycle, were monitored from storage oscilloscope displays. Spike timings were stored to 1 ms accuracy on computer disc: directional tuning curves (directions in 10 ° steps), averaged response histograms (50 ms/bin), and averaged spike firing (impulses/s) were derived on-line. Analyses of length summation and the derived plots of directional bias were made off-line.

Stimulus orientation and width were optimized. Since directionality may vary with stimulus velocity, z° optimal velocity was used in all cases except where video-recorded stimuli were presented. In the latter case, velocity was fixed at 4°/s, which represents a reasonable compromise for striate cells. Ocular dominance, together with classical tests for distinguishing complex from simple cells t6 (including sensitivity to moving randomly textured flelds6'l°A3), and preliminary tests of length summation and end-inhibition, were assessed. Thereafter the non-dominant eye was oc- cluded throughout.

Light or dark bars were presented on a CRT display (Hewlett-Packard 1304A) at 57cm, and were swept back- and-forth at optimal velocity against uniform or stationary, randomly textured backgrounds (256 x 256 elements sub- tending 10 x 10 ° square, generated at 50 frames/s; more recently 512 x 512 elements at 100 frames/s). 8 The presence of such a background has no influence, providing it remains stationary, t Average luminance was 1.1 log cd/m 2 and light and dark bars were, respectively, 0.3 log units brighter or 0.6 log units darker than the background. Animals either viewed this display directly, or video recordings of the same display presented on a monochrome TV monitor, centred on each cell's receptive field. When preparing the video recordings, the CRT display was masked by a 10 ° diameter circular window. Batches of stimuli were presented in pre-determined pseudorandom order.

Quantitative derivations of directional preference and tuning for oriented light or dark bars moving against stationary textured or uniform backgrounds were made manually or under computer-control. 6'7'~3 Standard (length- summating) cells, 4 especially, are more finely tuned for long than for short bars: thus, to achieve the most reliable fix on preferred orientation, essential for unambiguous assessment of length summation and directional bias, tuning was always assessed with long bars exceeding the receptive field length; in end-stopped cells the longest bar consistent with a reliable response was used. 2'8

Receptive fields were mapped as rectangular "minimum response fields". 3 The extreme locations of response as a long bar of optimal orientation entered and left the receptive field defined its lateral margins. Its ends were defined with a short bar whose trajectory was systematically altered until a response was barely audible.

Length summation was assessed quantitatively with bars whose orientation was constant but whose length was varied according to a pseudorandom sequence. In the case of the directly viewed CRT-display, a short bar of unvarying

length and of optimal velocity was presented alternately with a longer bar in batches of 10 or 16 trials, as a control for response variability. With video-recorded stimuli, bars of two different lengths were presented alternately (10 presentations of each at a fixed velocity of 4°/s). Each stimulus moved back-and-forth (1 s in each direction), fol- lowed by a 1 s pause. Resting discharge levels were mea- sured over the same number of cycles, with only stationary texture or a uniform background present. Each complex cell was classified as standard (length-summating), special (opti- mal response to short contours) or as intermediate (length summative properties intermediate between those of stan- dard and special complex cells), according to Gilbert's criteria 4 modified in light of our own experience. 2'8

Length summation data were replotted as length vs directional bias functions for each cell. Directional bias was defined as

(P - N)/(P - S),

where P and N were the response strengths (in impulses/s, without correction for resting discharge) in the preferred and null directions of motion, respectively, and S was the resting discharge level of the cell. Thus, a ratio of 1 implies that a cell is direction selective, with no response in the null direction; 0 that it is bidirectional (equal responses in either direction of motion across the receptive field). Ratios > 1 imply direction selectivity together with null suppression; direction-biased cells yield ratios between 0 and I; a negative value implies a reversal of bias.

RESULTS

Synopsis

The results are a subset of a large sample of simple and complex cells recorded from superficial and deep layers of area 17 of 15 adult cats o f either sex (mean weight 3.4 kg; range 2.5-4.2 kg). Length summat ion and directional bias were assessed in 81 complex cells, of which 31 were end-stopped to some degree- -34 special (18 end-stopped); 35 s tandard (10 end- stopped); 12 intermediate in properties (3 end- s topped)- - inc luding 56 cells whose length summat ion behaviour alone has been reported previously. 2'8 Data for two of the end-stopped complex ce l l s - -one spe- cial, one intermediate in character is t ics- -showed ex- treme variability and were discarded from the outset. Comparable data for 5 simple cells (3 end-stopped) are included for comparison. Table 1 summarizes these data for each functional class.

Variation o f direction selectivity with stimulus length

Figure 1 illustrates examples of three complex cells showing, respectively, no change, decreasing and increasing direction selectivity with increase in bar length. The common picture was that seen in Fig. I(A)-(B), especially amongst cells totally selective for direction and lacking a resting discharge. However, changes in direction selectivity with length could be quite dramatic, the cell o f Fig. I (C)-(D) being strongly biased for direction for short bars but ap- proaching bidirectionality for tong bars, whereas the cell o f Fig. I (E)-(F) was direction biased for short bars and direction selective for long ones. Of 79 complex cells, direction selectivity altered system- atically with length in 44% (35 cells) and was un-

Directional bias in complex cells 27

i , , , , , , i ~ , , #~1 r i r ,

i:

,

4~n3

°~ ~ 2" ~ ' ~ ' ~ ooo

~ ! ~ ~ ~ , , i i g

x o L x o ~ ................. , ............ :___._~

o

>~ ~ . ~ >~

~ g ~ ~ 1.4_ ; L.--J

i i i i i i i i I ~

2

E o

m - m

i morn

J i

," ~ i

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . I . . . . . . . . . . . . . ~ . . . . . . . . . . . . . . . . . . . . . . ÷ . . . .

t - - q i i i i i ~ i ~ i ~ i i I

( o ~ s / s ~ i n d ~ ) a s u o d s ~ a u ~ N

I

[ 1 ~ 1 1 1 1 1 1 1 1 1 1 1 1 1

o o m

m~

L o -o ii

c u o c

o

o o

n m

g

/

S i i i i i i i i

X#~^~og~as ~ o ~ 0

~-0 c

x o ®

u ~ < . on

i on~ cm

• v ~ o [ 9

L__J I ~ J

i i i ~ L i i i

, ~ 0 [.z.1 . .

~ r.z.l ¢~ ,,-% o.~

o e-. ¢~ J

o ~ , ~ ~ ~ , ~ - ~ 0 ~

~ . ~

~ g ~

~ ~ ~ - ' ~ .=

~ ~ .~ ~

~ 0 . ~ ,

• ~ ' ~ ~ .~ .-~

~ ~ 0 ~ r - ~

i ~ . ~

.~ ' .~ o ' ~ - , , ~=h

2x I’. HAMMOW and G S. V. MOIIAT

Table 1. Direction selectivity: dependence on stimulus length

Complex cells Standard Standard-H All standard

Special Special-H All special

Intermediate Intermediate-H All intermediate

Totals:

Number Direction selectivity vs length of cells No change/Change

‘5 IO 35

lb I7 33

Y 2

II 79

I2 I.3 h 4

IX I7

7 Y I4 3 21 I2

4 5 I I 5 6

44 35

Simple cells Simple 2 2 0 Simple-H 3 3 0 All simple 5 3 0

Suffix -H implies end-stopping (hypercomplexity)

x i 2 ? IO 7

5 4 3 0 X 4

3 -l

I 0 4 7

22 1;

changed in 56% (44 cells). Amongst complex cells,

increasing direction selectivity with increase in length was more prevalent (28%; 22 cells) than decrease in selectivity (16%; 13 cells). By contrast, direction

selectivity was independent of bar length in all five of

-_

.-_

Fig. 2. Length summation and direction selectivity in an end-stopped, direction-selective simple cell. Bar width 0.3’.

uniform background; all other conventions as in Fig. 1.

the simple cells studied for comparison (Fig. 2), whether they were inherently direction-selective or bidirectional.

There was no correspondence between a cell’s overt direction selectivity and its susceptibility to change of

directionality with stimulus length. Thus bidirec- tional or direction-biased cells were no more (or less) likely to show fluctuations of directional selectivity with length than direction-selective cells-even when the latter exhibited null suppression. Moreover. cells in all directionality groups (whether bidirectional, direction-biased or direction-selective) were equally likely to show length-dependent increases or dc-

creases in direction selectivity. Length summation and direction selectivity vs

length were examined for both light and dark bars in 14 cells. In all but two cases the length summation and dependence of direction selectivity on length were similar for stimuli of either contrast (see also Refs 8, II and 12).

Complex cell class dependency

The distribution of length dependency in direction selectivity for all classes of complex cells, including end-stopped members of each class, is shown in Table 1. With the following exceptions, there were no clearcut distinctions between the different functional groups of cells. Direction selectivity of standard and

intermediate complex cells was more likely to be affected by stimulus length (49 and 55% of cells, respectively) than was the case for special complex cells (36%). This was especially noteworthy if one distinguishes between end-stopped and non-end- stopped cells in each group. Direction selectivities of only a small minority of end-stopped special complex cells (18%) were susceptible to changes in stimulus length; in fact this was true to a lesser extent for end-stopped members of all classes of complex cells. In common with Gilbert,4 we noted a much higher incidence of end-stopping amongst special than amongst other classes of complex cells.

Directional bia

Our results show that. regardless of class. ap-

proaching hall’ of all complex cells show some degree

of dependency of direction selectivity on stimulus

length. However. there was no obvious correlation

bctwc~ each cell’s overt direction selectivit) (vk.

bidircctronal. direction-biased or direction-selcctivc).

or it\ susceptibility to change of directional bias. and

bar Icngth. Coupled with the fact that individual cells

from all complex-cell classes were affected, some

becominp mot-c. others Icss. direction-selective wirh

lengrh. it is itnplausihlc that length per .S(J can he

encoded bq a neuron’s direction selectivity.

For ach measurcmcnts to bc reliable. it is ob\i-

ou\ly csscntial for them to be made at precisely each

cell’\ optimal orientation. Measurements at wcn

slight11 non-optimal cwcntaCons might conccivablq

>iclti an cntircly difcrent result. This could aribc.

tirstl! hecause long bar\ are more likely to provide

s~mult;lncou> coverage of discharge centre and

flanking regions of the rcceptivc ticld than arc short

bar\ M hen presented other than at the cell’s optimal

orxnlalion. leading 10 a prcmaturc decrement of’

raponsc: \ccondl! beca~~se preferred and non-

prefcri cd directions in sonic cells are not I80 apal-1.”

Phirdlv. Ihe orientation selectivity of length sun-

mating cells (simple ccll~ and standard complex cells).

Airpens with incrcasc in bar length:’ “.” thus an

~iicread responxc level resulting from increase in

Icngth ma) hc partly offset by the greater response

dccrcmcnr ussoci:lU~ with mismatch in orientation

for lo11g than foi short bars. This factor might also

i-c\ult in coniplcu ccllz in ditti-rent cortical I~iiinac

hcing JitYcrcntiall> aKectcd, since thcrc is cvidcncc

thar aharpnes5 of tuning ror orientation is dictawd

partly by Iani~na.““’ ‘_ For this reason all our mea-

\urcmcnth v,ccl-c made at precisely the preferred oricn-

tatIon ~(II- each cell. and ail assessments oforientatlon

tuning \\cre made with long. rather than short, barb.

\Vhat of the special GISC of‘ end-stopped cells and

rhe comparat~vc 5rabili(> of their direction selectivity’!

Thcrc i\ indepcndcnt evidence which bears on this

tinding. Thus Orhan c’r ~1’~~” noted that end-zone

inhiblrion 14;~s pan-dircc~ional in end-stopped cells.

It might thus bc espcctcd to influence direction

sclectivtl! non-5pcclficall) for all orientations and

dll-ccrlonh of mo\cmcnt. However. the same au1hoi-s

;IIMI Icport end-/one inhibition to be maximal along

a h!pci-complex 0211‘5 axi orientation. operating onl)

111 Ihc prcfcrrcd direction of motion in sonic in-

slanca Morcobcr. home non-end-stopped direction-

hl;t\e.i ccllx may in f:lct be end-stopped in the null

dit-cctIc)n 01‘ motion alone. These fac,lctors imply Ihal

Icngh amimatlon must be greater in the noti-

pi-ct’crrcd than in the preferred direction in snmc

end-stopped cells. but actually the reverse in :I pro-

portion of non-end-stopped cclls~ results which

would Indeed predict Icnpth-depcndcnt \ ariation 01‘

directional bias. Other factors which might habe induced apparent

length dependency in dircchon &zcti\lry Include

driving cells inlo saluration. hcyond the linear phase

of the stimulus-~trcngth w r-csponx rclalionsh~p.

either because stimulus contrast \\:I$ \ct loo htgh.

because of length summation /MY SC’. or ;I ccmhinatwn

of both. In the data presented. nei1hcr explanation 15

particularly hkcl!. tirstlq because \+c r:irely drove

cells beyond 100 impulse\ s. which \\‘;I?, much helol\

their potcnU maximal tiring rates: secondly heca~~sc

stimuli were suitahl) restricted in contrast (~32 Eu-

perimcnlal Proccdurc\).

Notably. Ihe grcatcst \artarion 01’ dirc&on ~~lcc-

tivit;” Lvith lcnglh occurred for short bars. uhtch

elicited comparativclq ~+cah response\. irathcr than

for bars of optimal length. The pi-incipal cxplanatlon

for this 12. ol‘cour~c. Oiar genuine changes 111 rcsponsc

strength wrc grcarcr l’or shorr ham-\. lor \\hidi Icngrh

summation 1% a4 Ii iicx. rhan for Ionpr \~intuli.

Caution in intei-pretntion 1,. how\cr. ncccswr!, hcrc’

since an) nicasurc of direction selccri\it!. including

that \b hich \+c ;idopM. 15 inhercnll! LI~I-CII;I~IL’ in

cases of Lveak rcsponsc. The direction \clccrlvit;< in-

dcx is susceptible to frank mislntcrprctallon lilr short

bars whose Icngth\ arc subthrc\hcrld l’or ;I ccl1 /.ero

response neazisaril~ dtctalcs an iii&\ (~1‘ ICIO. Hut

especially in direction-sele~ti\~ cell\. c~cn the wcakc\t

of rcsponscs in rhc pt-cfcrrcd dircstton. hc)\\s\cr \llght

(e.g. at 0.35 and 0.5 in I’ip. I .A). ~ninii‘dt;t~cl~ r;ti\c5

the index to unit) without there l-~~ng. 111 rcalil!. an!

change of sctcctl\it!. With thi\ pro\i\o. all truly

direction-selecti\c tzcIl\ h~clded an ~n\ai-i;~n~ unit)

index (or greater. II‘ null supprc\\ton \\crc pre\ent).

c.p. Figs I(AJ. (R) and 71). I 131. In LTII\ u how

dircctlnn sclcctl\it? dccrc;i\ed \+ 1111 bar icngth. the

index apprcachcd ;I m;~\;~rn~l \aluc of unit\ t’oi- ,\horl

bars I\ host Icngth cwcctlcd thl-c4~olti. iVi,h ccl15

whose dirccrion \electi\lt\ :ncrc.~\cd \\llll IcnL$h.

howeher. for e*atiipk, tlic-ccl1 (\I I,ig I (I’) ;IIIC~ (f:).

the index \\;Is Iowc\t for ~OI-L lwi \.

30

2.

3.

4.

5.

6.

7.

8.

9.

10.

Il.

Ahmed B. and Hammond P. (1984) Length summation characteristics of complex cells in cat striate cortex, hi)\4 t-otwxi is the “special” vs. “standard” classification? J. Physiol.. Land. 353, 24P. Barlow H. B.. Blakemore C. and Pettipew .I. D. (1967) The neural mechanism of binocular depth dtscrmunatrorn J. Physiol., Lond. 193, 327 -342. Gilbert C. D. (1977) Laminar diflerences in receptive field properties of cells in cat primary visual cortex. .I. l’hv.ricJ Lond. 268, 391421. Hammond P. (1978) Inadequacy of nitrous oxide/oxygen mixtures for maintaining anaesthesia in cats: satisfactory alternatives. Pain 5, 143-l 5 I. Hammond P. (1978) Directional tuning of complex cells in area 17 of the feline visual cortex. J. Phy.~iol.. Lomb. 285, 47949 1. Hammond P. (1981) Simultaneous determination of directional tuning of complex cells in cat striate cortex for har and for texture motion. Exp. Bruin Res. 41, 364369. Hammond P. and Ahmed B. (1985) Length summation of complex cells in cat striate cortex: a reappraisal of the “special/standard” classification. Neuroscience 15, 639-649. Hammond P. and Andrews D. P. (1978) Orientation tuning of cells in areas 17 and 18 of the cat’s visual cortex. E-X/J. Brain Res. 31, 341.-3.51. Hammond P. and MacKay D. M. (1977) Differential responsiveness of simple and complex cells in cat striate cortex to visual texture. Exp. Brain Res. 30, 275-296. Hammond P. and MacKay D. M. (1983) Influence of luminance gradient reversal on simple cells in feline striate cortex. J. Physioi., Land. 337, 69-87.

12. Hammond P. and MacKay D. M. (1985) Influence of luminance gradient reversal on complex cells in feline striate cortex. J. Physiol., Lond. 359, 315--329.

13. Hammond P. and Smith A. T. (1983) Directional tuning interactions between moving oriented and textured stimuli in complex cells of feline striate cortex. J. Physiol., Lond. 342, 3549.

14. Henry G. H., Bishop P. 0. and Dreher B. (1974) Orientation, axis and direction as stimulus parameters for striate cells Vision Res. 14, 767-778.

15. Henry G. H., Dreher B. and Bishop P. 0. (1974) Orientation specificity of cells in cat striate cortex. J. Neuroph_v.Col. 37, 13941409.

16. Hubel D. H. and Wiesel T. N. (1962) Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. J. Physiol.. Lond. 160, 106-l 54.

17. Leventhal A. G. and Hirsch H. V. B. (1978) Receptive properties of neurones in different laminae of visual cortex of the cat. J. NeurophyCol. 41, 948-962.

18. Orban G. A., Kato H. and Bishop P. 0. (1979) End-zone region in receptive fields of hypercomplex and other striate neurones in the cat. J. Neurophysiol. 42, 818-832.

19. Orban G. A., Kato H. and Bishop P. 0. (1979) Dimensions and properties of end-zone inhibitory areas in recepttve fields of hypercomplex cells in cat striate cortex. J. Neurophysiol. 42, 833-849.

20. Orban G. A., Kennedy H. and Maes H. (1981) Response to movement of neurones in areas 17 and 18 of the cat: direction selectivity. J. NeurophJ,sio/. 45, 1059.--1073.

21. Peterhans E., Bishop P. 0. and Camarda R. M. (1985) Direction selectivity of simple cells in cat striate cortex to moving light bars, I. Relation to stationary flashing bar and moving edge responses. Exp. Bruin Res. 57, _512--522.

(Acwpwd I? Nowmber 1985)