Vtsion R$. VoL 11, pp. 833--$40. P ~ ' p m o n Press 1971. Printed in O ~ a t Britain.

THE TILT AFTER-EFFECT: A FRESH LOOK

F. W. CAMPBELLand L. M ~ l : m t
The PhysiologicalLaboratory, Cambridge

(Received 20 November 1970)

INTRODUCTION
THE NEUROPHYmOLOGICALstudies of HtmEL and WIESEL(1959, 1962, 1965, 1968) have shown
that, in the cat and monkey, there are neurons in the visual cortex which are sensitive to
the orientation of a bar, slit, or edge moved through their visual field. The selectivity of
these neurons to orientation has been measured in the cat (CAMPBELL, CLELAND,COOPER
and E~mOTH-CUGELL, 1968) and their selectivity has been compared with similar psycho-
physical measurements in the human (CAMPBELL and Ktn.IKOWSrd, 1966). More direct
evidence that the human visual system has an orientational mechanism similar to that in
the cat and monkey has been produced by Cam'SELL and MAF~t (1970). They used the
objective method of measuring the evoked potential from the visual cortex elicited by
repetitive presentation of stimuli.
The observations of Hubel and Wiesel indicated that there was no preferred orientation,
that is, the family of neurones each with its particular preferred orientation were distribu-
ted equally all round the clock-face. However, more recent studies by PgrnG~'w, NIKARA
and BISHOP(1968) have shown that among the "simple cells" close to the field of central
vision, there is a slight preponderance for the vertical and horizontal axes. MarFm and
CR~tPB~ (1970), using the evoked potential technique have shown that the human visual
system definitely has a greater response in these axes as compared with the oblique axes.
These objective findings agree very well with the numerous psychophysical studies on
various forms of visual activity measured in different orientations (see HOWAJ~D and
Tnm~LgrON, 1966, for review). It is known from the experiments of CAMrB~L, KULIKOWSra
and LEvr~soN (1966) that this phenomenon is not due to the optics of the eye, as the effects
of the optics of the eye can be by-passed by means of laser interferometry. MAF~I and
CAMPBELL(1970) also found that the human electroretinogram did not show any difference
between the vertical, horizontal and oblique meridians, although the orientational effect
was present when evoked potential recordings were made from the occipital scalp. Thus,
it may be concluded that these orientationaUy dependent effects are not due to the optics
of the eye and that they arise somewhat between the site of origin of the electroretinogram
and the visual cortex.
There are a number of effects which can be demonstrated psychophysically which suggest
that the vertical and horizontal axes are unique in the sense that they show properties which
are not common to other angles. We wondered whether some of these effects could be

l On leave from Laboratorio di Neurofisiolgiadel C.N.R., Pisa, Italy.

833
834 F, W. CAMPBELLAND L. MAFFEI

interpreted in terms o f m o d e m , more detailed knowledge o f neurophysiology. We chose to

study first the well k n o w n tilt after-effect which was first described by GmsoN (1933). This
effect has been studied subsequently in very great detail (see review by HOWARD and
TEMPtETON, 1966). Because o f conflict on the very points u p o n which we required accurate
information we have repeated some o f these experiments using the more suitable methods
which are available today.

i
i1111 I!itt111
Fxo. 1. See text for explanation.

To familiarize the reader with the p h e n o m e n o n which we are going to measure, Fig. 1
has been prepared. The reader should adapt to the upper left grating for 20 sec and then
view the lower middle grating. He will note that it is n o w tilted in the opposite direction.
He can verify that the effect is symmetrical by n o w adapting to the upper right grating.
The spatial frequency o f the adapting and test grating does n o t need to be similar, as he
can see by adapting to one o f the u p p e r oblique gratings and then viewing the grating o f
different frequency in the lower block. Indeed, a grating is not required to detect this adap-
tion effect as the vertical line in the lower block m a y also be tilted.

METHOD
The test grating was generated on the face of an oscilloscope using a modified television technique. The
rest grating subtended 2 =dia. The adapting grating was of high contrast and drawn on a card held in a
rotatable mount. It subtended 4 dia. The subject directed his gaze at the centre of the test, or adapting,
grating as required. About 20 sec of adaptions was used between each reading. The tilt of the test grating
was measured by rotating a fluorescent rod placed to one side of the visual axis, and just outside of the
part of the visual field which had been adapted. It is known (HowARD and TEMPLErON, 1966, Ch. 8),
and we confirm, that the adaption effect is confined to the visual field which has actually been adapted; we
took care to ensure that the rod was always outside this adapted region of the field. The fluorescence of the
rod was activated by means of ultrav/olet light. The subject turned the rod until it appeared parallel with
the test grating, the centre of which he was inspecting. The room was sufficiently dark so that the subject
could only see the fluorescent rod but none of the rooms furnishings while he was inspecting the test grating
(luminance 60 cd/MZ). The rod (2 long by 10' width) was attached to a linear potentiometer; the voltage
generated across the potentiometer could be read on command by a PDP-8 computer. The computer cal-
culated and printed the necessary statistical values.
 The Tilt After-effect: A Fresh Look 835

RESULTS
Description of the basic effect
The test grating (spatial frequency 12 c/deg) was kept vertical throughout the experiment
and the orientation of the adapting grating (12 c/deg) was changed in small steps.
The results are shown in Fig. 2. It can be seen that from0 to 8 the tilting effect increases
rapidly and linearly, reaching an angle of apparent tilt of 4 . That is, the gain of the tilt
effect over this range is--0.5. As the angle between the test grating and the adapting grating
is further increased the tilt effect diminishes slowly and, to a first approximation, exponen-
tiaUy, over the range observed. The experiment was now repeated with the test grating
oriented horizontally. Very similar results were obtained.

50 -40 -30 -20 -|0 LO 20 30 40 so

Orientation of the adaptinq (Jeatinq, dec]

F[o. 2. The test grating was kept vertical (0 ) and its apparent tilt was measured for different
orientations of the adapting grating. Anticlockwise(--) and clockwise (+). Each point is the
mean of 10 observations. The continuous line is the best symmetrical curve that could be
fitted by eye.

The experiment was then repeated with the test grating placed in an oblique axis (45).
No apparent tilt was observed. A negative result was also obtained if the test grating was
in other oblique positions over a range of 4-30 . That is, no apparent tilt occurs unless the
orientation of the adapting test grating is very close to either the vertical or horizontal.
The reader may verify this negative finding by rotating Fig. 1 into an oblique orientation.

Binocular transfer
GmsoN (1933) found almost complete transfer of figural after-effects when the adapting
pattern stimulus was presented to one eye and the effect was observed with the other eye.
We have repeated this observation on the tilting effect and the results are shown in Fig. 3.
On this occasion, we only made the observations in one quandrant and a comparison of
the monocular interocular results are shown in the same figure. Clearly there is no signifi-
cant difference in the two sets of results, so that it can be concluded that there is complete
transfer from one side to the other.
The reader can demonstrate this point readily by viewing Fig. 1, first with one eye for
an adaptation period and then viewing the test object with the other eye.
836 F . W . CAMPBELLAND L. M.AFFEI

o Io 20 30 40 50
Orientation of the adapting grating, deg
FIG. 3. The ( 0 ) represent the results obtained when the test grating was viewed with the same
eye that was adapted. The ( 0 ) were obtained when the test grating is viewed with o n e eye
while the other was adapted. Each point is the mean of 10 observations.

The indirect effect

If the test object is vertical it is possible to cause an apparent tilt by adapting to a
grating close to the horizontal and vice versa. Thus, gratings at right angles seem to influence
each other.
Gmso~ and RaDN~ (1937) originally noted that exposure to one orientation produced
a tilt after-effect in another 90 apart. Mo~Ayr and MISTOVlCH(1960) confirmed this finding
although earlier KO~ER and WALLACH(1944) and ~ C E and BE~a~DSLEE(1950) failed
to find this indirect effect. This doubt lead us to measure the indirect effect as a function of
angle.
The test grating was vertical. The adapting grating was horizontal and was moved in
steps from the horizontal axis (90 ) towards the vertical. The results are shown in Fig. 4.

)o 80 ~o
Orientation of the adaptin9 qrating, de9
FIO. 4. The test grating was vertical. The adapting grating was varied on one side of the
horizontal meridian, n = 10.
 The Tilt After-effect: A Fresh Look 837

The effect is smaller by a factor of about a half but the shape is similar to the normal
effect, as is illustrated in Fig. 2. This experiment was repeated with similar results in 5
subjects.

Precision of orientation judgement

There have been many studies on the precision with which we can set a reference line
to a particular orientation (see HOWARD and TEMPLETON, 1966). We have re-determined
this ability with the same luminous line, used in the previous experiments.
A reference card was visible to the subject. On this card is drawn a fan of lines with 10
difference in tilt between each line. Each tilt angle was numbered. The subject was instructed
to inspect a particular orientation. He then transferred his gaze to the luminous line and
adjusted it until it appeared to have the same orientation as the requested orientation. He
was free to refer as often as desired to the reference card containing the fan of orientation.
Only the fan of lines and the fluorescent rod were visible to the subject. The requested

deg
3

F[o. 5. The standard deviations obtained by setting a line to a specificorientation. The results
are displayed on polar coordinates.

tilt was selected randomly by the computer and when the angle had been set by the subject
he pressed a switch which instructed the computer to read the angle set. Twenty observa-
tions were made at each angle and the standard deviation was computed. These S.Ds are
plotted on polar coordinates in Fig. 5. It can be seen that the S.D. for oblique angles is very
much greater (about 3) than that found for the vertical and horizontal axis (about 20').
We also repeated the experiment with the subject lying horizontally on the floor and
looking upwards at the luminous line. Here he was asked to set the line vertically, horizon-
tally and at 45 using his body as the reference as he was now deprived of gravity as a meaning-
ful reference. The S.Ds were, horizontal 1.7 vertical 1-4 and oblique 3-6.

DISCUSSION
From the last experiment we may conclude that, when the subject is effectively deprived
of the clue of gravity, the judgement of the vertical and horizontal axes is much less, for
the standard deviation changes from about 20' to about 1.5 . However, for the oblique
838 F . W . CAMPBELLAND L. MAFFEI

angles, there is no significant difference caused by change in the direction of gravity, for
the standard deviation remains at about 3. Even so, when the subject is deprived of the
clue of gravity, judgement of orientation is worse in the oblique meridians compares with
the vertical and horizontal by a factor of about 2. Thus, it appears that we have two distinct
mechanisms: one is of very high precision, when the reference of gravity is available, the
other is not.
The latter might be a property of the structure of the visual nervous system, for it could
be argued, on the grounds of its small magnitude, that it is related to the mechanism which
accounts for the better visual resolving power in the vertical and horizontal meridians which
is comparable in magnitude. This effect cannot have a psychological explanation such as,
"we are used to seeing more vertical and horizontal things in our environment", for it has
been shown objectively to exist by using an evoked potential technique (MAFFEI and
C~'B~.LL, 1970). In our account of this evoked potential experiment we concluded that
these electrophysiological findings might be due to a greater number of orientationally
selective neurons being devoted to discrimination in the vertical and horizontal meridians,
as indeed has been found for cortical neurons subserving the central part of the visual field
in the cat (PEI"TIGREWet aL, 1968). However, this conclusion may not be too secure for we
have since had the opportunity of examining statistically the distribution of orientations of
all the neurons investigated by HUBELand WIESEL(personal communication) in the monkey
visual cortex. The distribution does not show any preferred orientation for horizontal and
vertical orientations. It could be that there are real species differences between the cat,
monkey and man: behavioural experiments would be required to throw further light on this
problem.
An alternative explanation for the greater precision in the vertical and horizontal orien-
tations might be that the neurons subserving these axes might have a greater angular
selectivity, as indeed, was shown by CAMPBELLand KULIKOWSKI(1966) using a psycho-
physical masking method. They found that the half width of the effect was 12 for the verti-
cal and 15 for the oblique orientation.
Now the tilt after-effect investigated here does not occur at the oblique orientations
although we are fairly certain in the human that there are neurons subserving oblique
orientations, just as there are in the cat and monkey. It could be argued that the tilt after-
effect is present at the oblique positions but that the large standard deviation found in the
judgement of the tilt swamps the effect. However, this is unlikely for one should be able to
detect the effect by making a sufficiently large number of observations. Keeping this diffi-
culty in mind we have tried very hard to demonstrate its presence in the oblique orientations
and have failed.
Another special characteristic of the tilt after-effect is that it can be induced with a
grating of one spatial frequency and its presence detected equally well with a grating, or
indeed a single line, of quite a different spatial frequency (see Fig. 1). This observation could
be accounted for if the mechanism responsible for orientational selectivity occurs before
the processes leading to spatial selectivity. This need not imply that the entire mechanism
for spatial analysis is more central than the mechanism responsible for orientational selectiv-
ity. For example there is some evidence that the receptive fields of ganglion cells cover a
range of sizes (KUFrLER, 1953). Moreover, CA~XPBELLet al. (1969) found that the spatial
frequency response characteristics of the geniculate neurons covers a range of three to four
octaves of spatial frequency. These findings apply to the cat as well as the squirrel monkey
(CActi'BELL et aL, 1969).
 The Tilt After-effect: A Fresh Look 839

A remarkable property o f the tilt after-ffect is t h a t it transfers completely from one

eye to the other. As far as we k n o w this is the only after-effect showing complete inter-
ocular transfer. F o r example, the adaption effect which has been used psychophysically
to uncover the channels which are selectively sensitive to b o t h orientation and spatial
frequency is only partially transferred f r o m one eye to the other (BLAKEMOREand CAMPBELL,
1969) and this is further evidence that we are dealing with a different mechanism in these
tWO cases.
During editorial correspondence, Dr. G. B. A r d e n pointed o u t that we h a d omitted to
do the easy and interesting experiment o f seeing what happens to the tilt after-effect when
the observer is lying horizontally. The reader can experiment for himself by affixing Fig. 1
to the ceiling and viewing it f r o m the appropriate horizontal posture. Six subjects, who
readily reported the after-effect in the vertical posture, also reported an effect with the same
degree tilt when in the horizontal posture. We m a y therefore draw the additional conclusion
that the clue o f gravity is not an important factor in causing the tilt after-effect.
Acknowledgement--F.W.C. is supported by a grant from the Medical Research Council.

REFERENCES
BLAKEMOI~,C. and CAMPBELL,F. W. (1969). On the existence in the human visual system of neurons selec-
tively sensitive to the orientation and size of retinal images. J. Physiol. 203, 237-260.
CAMPBELL F. W., CLELAND,B. G., COOPER,G. F. and ENROTHoCUGELL,C. (1968). The angular selectivity
of visual cortical ceils to moving gratings. J. Physiol. 198, 237-250.
CAMPBELL F. W., COOPER,G. F. and E~So~-CuoELL, C. (1969). The spatial selectivity of the visual cells
of the cat. J'. Physiol. 203, 223-235.
CAMPBELL F. W., COOPER,G. F., RO~.qON,J. G. and SACHS,M. B. (1969). The spatial selectivity of visual
ceUs of the cat and squirrel monkey, d. Physiol. 204, 120-121.
C ~ n E L L F. W. and KULmOWSgLJ. J. (1966). Orientational selectivity of the human visual system. J.
Physiol. 187, 437-445.
CAMPBELLF. W., KULIKOWSKI,J. J. and LEVINSON,J. (1966). The effect of orientation on the visual resolu-
tion of gratings. J. Physiol. 187, 427-436.
CAMPBELL F. W. and M m m , L. (1970). Electrophysiologlcal evidence for the existence of orientation and
size detectors in the human visual system. J. Physiol. 207, 635-652.
GmsoN, J. J. (1933). Adaptation, after-effects, and contrast in the perception of curved lines. J. exp. Psychol.
16, 1-31.
Gtaso~, L L and RAring, M. (193"0. Adaptation, after effect, and contrast in the perception of tilted lines--I.
Quantitative studies. J. exp. Psyehoi. 20, 453-467.
Howxm~, I. P. and TEMPLFrON,W. B. (1966), Human Spatial Orientation, John Wiley, New York.
H~EL, D. H. and WmSEL,T. N. (1959). Receptive fields of single neurones in the cat's striate cortex. J.
Physiol. 148, 574-591.
HUnEL, D. H. and WmSEL,T. N. (1962). Receptive fields, binocular interaction and functional architecture
in the cat's visual cortex. J'. Physiol. 160, 106--154.
HUBEL,D. H. and WIESEL,T. N. (1965). Receptive fields and functional architecture in two nonstriate visual
areas (18 and 19) of the cat. J. Neurophysiol. 28, 229-289.
HtmEL, D. H. and WmSEL,T. N. (1968). Receptive fields and functional architecture of monkey striate
cortex. J. Physiol. 195, 215-243.
KOHLEg,W. and W~d.L^CS, H. (1944). Figural after-effect: An investigation of visual processes. Prec. Am.
phil' Soc. 88, 269-357.
KUFI:LER,S. W. (1953). Discharge pattern and functional organisation of mammalian retina. J. Neurophysiol.
16, 37-68.
MAFFEI, L. and CAMPBELL,F. W. (1970). Electrophysiologlcal locaUzation of the vertical and horizontal
coordinates in the human visual system. Science, N.Y. 167, 386-387.
MogAtcr, IL B. and MLs'rowcH, M. (1960). Tilt after-effects between the vertical and horizontal axes.
Percept. motor. Skills 10, 75-81.
l~Trmasw, J. D., Nxr.xaA, T. and BisHop, P. O. (1968). Responses to moving slits of single lines in the striate
cortex. Exptl. Brain Res. 6, 373-390.
PRENTICE,W. C. H. and BEARDSLEE,D. C. (1950). Visual normalization near the vertical and horizontal.
d. exp. Psyehol. 40, 355-364.
840 F . W . C ~ a ~ L L AND L. MArnu

Ai~tract--A h/gh contract grating was used to induce the tilt after-effect. It was found to
occur only close to the vertical and horizontal orientations. The interocular transfer of this
effect is complete. Judgement of the vertical and horizontal orientation as measured by
determining the Standard Deviation at a number of orientations b much more precise even
when the cue of gravity is removed. All the characteristica of the tilt after.effect cannot be
accounted for by adaption of neurones selectively sensitive to orientation, although they may
well be involved.

Rfn~um~--Une grille tr~s fine a ~t~ utilis~e pour produire une inclinaison par r~percussion.
On a trouv~ que cet effet se protiui.~it seulement pr;~ des orientations verticale et hori-
zontale. Le transfert interocula~ de cet effet est complet. Le jugement de l'orientation
verticale et horizontale, mesur~e en d~terminant la D~viation Standard a un nombre d'orienta-
tions, est beaucoup plus pr~is m~ne qtmnd l'index de gravit~ est 6:art~. Toutes les carac-
t~ristiques de l'effet d'inclinaison qui suit, ne peuvent pas etre e x p l i q t , ~ par l'adaptation des
neurone s~iectivement sensibles/t rorientation, qunlqu'ils pourraient bien ~tre impliqu~.

Z u s a n m a e a f ~ . ~ - - M a n verwendete ein stark zusammenziehendes Beugungsgitter zur

Erzeugung der Kipp-Nachwirkung. Man land, dass diese nut nahe den vertikalen und hori-
zontalen Orientationen auftrat. Die zwiscben den Augen stattfindende Wirkung dieses Effektes
ist komplett. Beurteilung der vertikalen und horizontalen Orientierung bemessen nach der
Bestiramung der Standardabweichtmg einer Reihe von Orientationen ist viel pr-~ziser, selbst
nach Entfernung des Gravitationssigna~. Nicht alie charakteristischen Merkmaie der Kippo
Nachwirkung k6nnen dutch Anpa~ung yon Neuronen, die gegenfiber Orientierung selektiv
sensitiv sind, erklart werden, obwohl es leicht m6glich ist, dass sie etwas damit zu mn haben.

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