Download Sequence regularity and geometry of orientation columns in the

Sequence Regularity and Geometry of Orientation Columns
in the Monkey Striate Cortex
DAVID H. HUBEL A N D TORSTEN N. WIESEL
Department of Nrurobiology, Hnrvard Medical School, 25 Shnttuck S t r r e t ,
Boston, Massachusetts 021 15
ABSTRACT
The striate cortex of the macaque monkey is subdivided into two
independent and overlapping systems of columns termed “orientation columns”
and “ocular dominance columns.” The present paper is concerned with the orientation columns, particularly their geometry and the relationship between successive columns. The arrangement of the columns is highly ordered; in the great
majority of oblique or tangential microelectrode penetrations the preferred orientations of cells changed systematically with electrode position, in a clockwise or
counterclockwise direction. Graphs of orientation vs. electrode track distance
were virtually straight lines over distances of up to several millimeters; such
orderly sequences were often terminated by sudden changes in the direction of
orientation shifts, from clockwise to counterclockwise or back. The orientations at
which these reversals occurred were quite unpredictable. Total rotations of 18%
360” were frequently seen between reversals. In tangential or almost tangential
penetrations orientation shifts occurred almost every time the electrode was
moved forward, indicating that the columns were either not discrete or had a
thickness of less than 25-50 p , the smallest order of distance that our methods
could resolve. In penetrations that were almost perpendicular to the surface, the
graphs of orientation vs. track distance were relatively flatter, as expected if the
surfaces of constant orientation are perpendicular to the cortical surface. S t e p
wise changes in orientation of about 10” could sometimes be seen in perpendicular penetrations, each orientation persisting through several clear advances of
the electrode, suggesting a set of discrete columnar subdivisions. The possibility
of some kind of continuous variation in orientation with horizontal distance along
the cortex was not, however, completely ruled out. Occasionaliy a highly ordered
sequence was broken by an abrupt large shift in orientation of up to 90”. Shifts
in ocular dominance occurred roughly every 0.25-0.5 mm and were independent
of orientation shifts. In multiple parallel penetrations spaced closer than about
250 p the slopes of the orientation vs. track distance curves were almost the
same; reconstruction of these penetrations indicated that the regions of constant
orientation are parallel sheets. On crossing perpendicular to these sheets, a total
orientation shift of 180” took place over a distance of 0.51.0 mm. Column thickness, size of shifts in orientation, and the rate of change of orientation with distance along the cortex seemed to be independent of eccentricity, at least between
2 ” and 15” from the fovea. A few penetrations made in area 17 of the cat and in
area 18 of the monkey showed similar orderly sequences of receptive-field orientation shifts.
In the monkey striate cortex there exist
two independent and overlapping systems
of columns which we have termed “orientation columns” and “ocular-dominance
columns” (Hubel and Wiesel, ’68). The
ocular-dominance columns are parallel
sheets or slabs arranged perpendicular
to the cortical surface subdividing it into
a mosaic of alternating left-eye and rightJ COMP. N E U R . ,1 5 8 . 267-294.
eye stripes 0.25-0.5 mm in width (Hubel
and Wiesel, ’72). For the orientation columns the geometry is less clear, though
we have had indications that they are
slab shaped. The present paper is concerned in part with this question. The
main subject, however, is the degree to
which the orientation columns are ordered. As the cortex is explored with a
267
268
DAVID H. HUBEL AND TORSTEN N. WIESEL
tangentially or obliquely moving electrode, stimulation could be heard on the audio
the sequence of ocular-dominance col- monitor.
The electrode was advanced in steps of
umns is obviously back and forth from
one eye to the other, since there are by 25-50 p , and a t each advance the redefinition only two kinds of ocular-dom- sponses were checked for changes in optiinance columns. For the orientation col- mal stimulus orientation. Steps smaller
umns one can distinguish something like than 25 p usually did not result in a
18-20 possible orientations, and it is not change of optimal orientation or of electritrivial to ask whether the electrode en- cal activity, either because the uncoated
counters a random or ordered sequence. tip length was 25 p or more, or because of
We have previously had hints that the col- the inevitable stickiness in the movement
umns were highly ordered (Hubel and Wie- of the electrode relative to the tissue. Obsel, '63, '68) and the results to be described viously these factors impose a lower limit
make it very clear that this order is the rule on the size of the columns that can be resolved.
rather than the exception.
We stimulated routinely by sweeping a
slit of white light of variable length and
METHODS
width across the receptive field in different
The series consisted of nine macaque orientations. When necessary we used dark
monkeys (rhesus and stumptail) one to bars or monochromatic slits. As the electhree years of age, and one cat. Of the nine trode advanced through the cortex each
monkeys seven were normal, one had long- new optimal orientation for activating sinstanding monocular blindness, and one had gle cells or groups of cells was recorded as
artificial strabismus from birth. The cat a line drawn on the receptive field chart
also had strabismus from birth. The total (fig. 1). The accuracy in estimating optinumber of cells recorded in monkeys was mal orientations varied from cell to cell,
1410, in 45 penetrations.
from roughly i 2-3" a t best, to i 5-10'
Most penetrations were made from the for less sharply tuned cells; in layer IV C
convexity of the occipital lobe, 2 to 7 mm most cells lack orientation specificity. Oriposterior to the 17-18 border and about entations were plotted against micrometer
10-15 mm lateral to the midline. This cor- readings of electrode position, with a new
responds to a region of visual field 4-10'
point marked each time the orientation
below and out from the fovea. Four pene- changed or each time any change in electrations were made f a r lateral, in the corti- trical activity made it clear that the
cal region representing the fovea, and two electrode had advanced. To determine
were made in the buried calcarine cortex, orientation we occasionally used a PDP-12
with fields 12" and 18" from the fovea. In computer to produce a graph of average reone experiment five penetrations were sponse vs. orientation, generating the slit
made in area 18, in the posterior bank of electronically on a television screen. This
the lunate sulcus about 10 mm from the method took much longer, and the usual
mid-sagittal plane (fig. 12). To help recon- minute-to-minute variations in responsivestruct the electrode tracks one or more elec- ness of the cells tended to make the curves
trolytic lesions were made in each penetra- broader and noisier. We concluded that
tion.
for both speed and for precision it is hard
Methods for animal preparation, stim- to beat judgements based on the human
ulation, and recording were generally those ear. Certainly a curve such as the one in
described in previous papers (Hubel and figure 2 could not have been obtained with
Wiesel, '68). Since i t was important to re- computer averaging methods before the
cord activity continuously as the electrode authors reached the age of mandatory readvanced, we made the tungsten electrodes tirement.
slightly coarser than usual, with 25-35 p
For binocular cells in which the two eyes
of uncoated tip rather than 15-25 p. With were equally effective or almost so (groups
such electrodes many isolated units were 3, 4, 5 . . . Hubel and Wiesel, '62), orienstill recorded in each penetration, but back- tation was determined separately for the
ground activity was more plentiful, with two eyes. For cells dominated strongly by
fewer gaps during which no responses to one eye (groups 1, 2, 6, 7) only one point
ORIENTATION COLUMNS I N MONKEY STRIATE CORTEX
269
corresponding to the dominant eye was one before, with steps that were small and
plotted. Open circles in the graphs repre- fairly uniform. At cell No. 111 the right
sent contralateral eye, closed circles, ipsi- eye suddenly became ineffective, and sublateral. Thus a n idea of the dominant sequently recorded cells were all strongly
eye and the degree of binocular interaction dominated by the left eye. The sequence,
can be obtained from the graphs at a however, continued in a counterclockwise
glance. When the orientations of a binoc- direction without interruption.
ular cell consistently differed in the two
These results are shown graphically in
eyes by a measurable amount (as in fig. 6, figure 1B. Orientations are plotted against
for example), the discrepancy could be ac- electrode-track distance in millimeters. In
counted for by a relative rotation of the plotting orientations, 0" is taken as vertical, angles clockwise up to 90" are desigparalyzed eyes in the equatorial plane.
After perfusion of the brain with 10% nated as positive, counterclockwise to 89
formol saline the occipital lobes were em- as negative. The first cell in the sequence
bedded in celloidin, cut in the parasagittal thus had an orientation of + 32". Track
plane at 25 p , and stained with cresyl distances are taken directly from the miviolet. The angle of the electrode track was crometer advancer readings, with zero as
measured in the histological slides either the depth at which unit activity was first
with respect to the cortical surface and the encountered.
The graph, like others obtained in this
layers or by taking the complement of the
angle made with the radial fascicles. In series, showed a high degree of regularity,
estimating this angle a n error is introduced and indeed a linearity, over long distances.
by sectioning the brain in the parasagittal Almost every 25-30 p advance of the elecplane rather than in a plane perpendicular trode was followed by a fairly constant small
to the surface, but this was small in pen- shift of about 10" in the optimal stimulus
etrations that were within 10-15 mm of the orientation. Since any particular orientamidline. Small errors in estimation of track tion could be measured only to the nearest
angles were important only in nearly per- 2-5" it was at times hard to be sure that a
pendicular penetrations, and then only in shift had actually occurred, but once the
calculations involving estimates of the hori- slope of the curve had been established the
zontal component of track distance. Num- orientation arrived at after several adbers based on such calculations are omitted vances in 25-30 p steps was predictable
with surprising accuracy.
from table 1.
AS pointed out in the method section, an
RESULTS
advance of the electrode by a substantially
Regularity of orientation columns
smaller distance, such as 15-20 p , often
In this study the main finding was the did not result in a n orientation shift, but
high degree of order in the arrangement of with such a small advance it was difficult
orientation columns. For many years our to be sure the electrode had moved relative
only good example of this order was a single to the tissue. Since most 2 S 3 0 p advances
experiment in a spider monkey (Hubel and of the electrode did result in orientation
Wiesel, '68, fig. 9), but since we began to shifts the regions of constant orientation
use lower impedance electrodes and the were obviously that size or smaller. Thus
plotting procedure described below we have the distances between observed shifts in
seen a high degree of order in almost every orientation, or their horizontal components
penetration.
("horizontal distance/shift" in table I),
Figure 1A shows a n example of a typical represent an upper bound to the thickness
ordered sequence in a very oblique penetra- of the columns, and not necessarily the
tion in a normal monkey. The first cell or true values. This should be kept in mind
group of cells in the sequence (No. 96 in in interpreting figures for the distance bethe experiment) strongly favored the right tween orientation shifts, or the number of
(ipsilateral) eye and had a 1 o'clock-7
degrees for each orientation shift, given in
o'clock receptive-field orientation. The next the present descriptions and in table 1. The
14 (Nos. 97-110) were all strongly domi- possibility that orientation may vary in
nated by the right eye and had the orienta- some sense continuously with horizontal
tions shown, each counterclockwise to the electrode movement is taken up in the disO
270
DAVID H. HUBEL AND TORSTEN N. WIESEL
.
If
rf
right eye
I I' l /
left eye
/
96
1
lo
,
96
101
99
100
Fig. 1 A Normal 2-3 year-old monkey. Observations during a n oblique microelectrode penetration through striate cortex. The drawing was made on a sheet of paper affixed to the tangent
screen 146 cm from the monkey. The eyes converged slightly so that the visual axes crossed,
with the left and right foveas ophthalmoscopically projected as shown (1 f and r 0. The receptive fields of 22 cells or clusters of cells were distributed through the regions marked with interrupted circles, 3" below and 3" to the left of the foveas. The first cell in the sequence, NO. 96
in the experiment, had an orientation 32" clockwise to the vertical, and was influenced from
both eyes but more strongly from the right (ipsilateral). Cells 97-110 were likewise strongly
dominated by the right eye; at No. 111 there was an abrupt switch to the left (contralateral)
eye, which dominated for the rest of the sequence (same penetration a s in fig. 8,A,D). (Experiment No. 5).
cussion, but here it may be well to point struction of figure 1C. The sequence was
out that 25-30 p is close to the dimensions part of a longer one described in figure 8D.
of a cell body, so that the column widths The span of 158" was covered in 22 shifts,
are already close to the lower limit. As giving a mean orientation shift of 7.2" k
shown below, the distance a n electrode 2.8" (S.D.), (Linear coefficient of correlatraveled between shifts in orientation was tion, 0.98). The 22 shifts in orientation
large enough to be measurable in nearly took place over a distance of 0.59 mm,
perpendicular penetrations, but then the giving an average distance between shifts
horizontal component of the distance be- of 27p, or 25 p in terms of distance parcame critically dependent on the angle be- allel to the cortical surface. This is equivtween electrode and cortex, and could not alent to 40 shiftdmm horizontal excursion.
Since the radial column-like bands of cells
be accurately estimated.
The part of the electrode track in which seen in Nissl-stained transverse sections of
the sequence of figure 1 occurred is shown striate cortex are separated by intervals
between the arrows in the track recon- of about this order of magnitude we thought
ORIENTATION COLUMNS IN MONKEY STRIATE CORTEX
-
271
it might be interesting to compare the
sizes directly. Figure 1 D shows a photomicrograph of the cortex with two lesions
made before and after the sequence of 22
shifts; the part of the track in which the
sequence occurred is indicated by arrows.
901
P
p3
I
1'0
112
1'6
1'4
TRACK DISTANCE
-
1'8
mm
Fig. 1B Graph of orientation vs. track distance
for the sequence of figure 1 A . I n plotting orientations, O o is vertical, angles clockwise u p to 90" are
positive, counterclockwise to 89', negative. Closed
circles, ipsilateral (right) eye; open circles, contralateral (left) eye. Track distance is taken from micrometer advancer readings.
Fig. 1C
\'
,,\*O
Reconstruction
,
.
I
+c
*
of the electrode track.
Electrode entered the striate cortex 8 m m behind
the lunate sulcus in the parasagittal plane, 10 m m
to the right of the midline, intersecting the surface
at 20". The sequence described here was recorded
between the two arrows. Circles represent electrolytic lesions. Anterior is to the right.
Fig. I D Photomicrograph of a Nissl-stained section through the two lesions and the electrode track. The track was visible only with dark-field illumination. The sequence of 22 orientation shifts occurred between the two arrows, within which space roughly 32 vertical bands of
cells c a n be counted.
2 72
DAVID H. HUBEL AND TORSTEN N. WIESEL
\
-30.
,-60.
.. .. ..
0
-
90.
.
, 60.
E
Z
QI2
Z
w-
1
30.
I
O.
. '...
0.
\
-30.
8 ,
-60.
-
90.
,
60.
1
30.
Fig. 2 A Graph of orientation vs. track distance for a n oblique penetration through striate
cortex in a normal monkey. Note the reversals in direction of orientation shifts, the first two of
which bracket a long sequence spanning 267O. (Experiment No. 7.)
(The track could only be seen with darkfield illumination.) The bands are not
sharply defined and can be counted only
very roughly, but in this part of the track
there appear to be about 32, or 54 bands/
mm.
Reversals in the direction of rotation
were seerl in about half of the penetrations
in the series. Several examples of such reversals are shown in figure 2, a graph from
a highly regular penetration in a normal
macaque monkey. Here one long clockwise
progression spanning 188" in 17 orientation shifts (average l l. l "/shift) was followed by a n even longer counterclockwise
rotation through 267" in 26 shifts (10.3'1
shift). This in turn was followed by two
shorter sequences. The total number of orientation shifts in the 2.2 mm track was
53, or 24 shiftslmm of horizontal excursion.
The number of radial bands of cells counted
along the electrode track was about 110,
giving 50 bands/mm.
Throughout almost the entire penetration the ipsilateral eye (closed circles) was
strongly dominant, though the contralatera1 eye was able to influence most of the
cells. Towards the end of the penetration
the dominance began to change, with a
few cells influenced about equally from the
two eyes, and by the very end the contralateral eye had become dominant. The
relationship between orientation columns
and ocular-dominance columns is considered below.
The regularity shown in these two examples was typical. Within any progressive
sequence, clockwise or counterclockwise,
the slope of the curve was generally fairly
constant. The total rotation taking place
before a reversal in direction of rotation
was highly variable, but the majority of
uninterrupted spans were over loo", onethird exceeded 200°, and a few were over
300". Many linear sequences were cut
short, not because of a reversal in direction
273
ORIENTATION COLUMNS IN MONKEY STRIATE CORTEX
Fig. 2B Reconstruction of the electrode track,
which entered the striate cortex 10 m m behind
the lunate sulcus and 10 m m to the right of the
midline, making a n angle of 7' with the surface.
Section is parasagittal. One lesion was made a t the
end of the 2.2 mm penetration. Receptive fields
were 1 below and 7.5' to the left of the fovea.
of rotation, but because the penetration
was terminated or entered white matter or
layer IV C (in which most cells have no
orientation specificity). The angles at which
reversals occurred were quite unpredictable, there being no tendency for any particular orientations, such as vertical or
horizontal, to be favored as points of rever sal .
Though most of the sequences were regular, isolated large jumps in orientation
did occur. Some of these may simply have
reflected a sudden movement forward of
the electrode after sticking relative to the
tissue, but others were certainly genuine.
An example of a pair of breaks in the order
of a sequence is shown in figure 3 from a
penetration described further in another
context below (fig. 8C). Here the orientation had been systematically changing in
a counterclockwise direction when suddenly there was a 70" counterclockwise jump,
followed by a short regular clockwise sequence and then a second counterclockwise
jump of 105". The previous counterclockwise sequence was finally resumed with
the same slope, just a s though it had never
been interrupted. At this point the electrode was pulled back slowly and then
readvanced, whereupon the entire sequence
was reproduced, making it almost certain
that the jumps were not in some way related to uneven electrode movements.
0,
I
-
0
'
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.. .
.
x
O
-60-
- - 900
P
+
5,
60-
Ly
8
30.
.
I 0-
o
o
0 0
- 0
\ -30
0
0'2
0!4
016
0!8
110
2 74
DAVID H . HUBEL AND TORSTEN N. WIESEL
several tangential penetrations through
some small region of cortex in various
directions, but for the present the idea was
abandoned because of the difficulties in
finding a suitable plane of sectioning for
histological reconstruction. The results of
making multiple parallel penetrations are
taken up below.
In tangential penetrations individual
shifts in orientation tend to be obscured in
orientation-vs.-distance curves because of
limitations in resolution along the distance
axis. On the other hand a penetration that
is deliberately made almost normal to the
surface should intersect the columns at a
very small angle and pass through relatively few of them; the curve should be relatively flat, and individual shifts should be
further apart and consequently more easily
seen.
The two penetrations of figure 4 were
made about 1.5" from the foveal representation of the right hemisphere in a normal
monkey. In penetration 3 (fig. 4B), which
was almost normal to the surface, the slope
of most of the curve was - 54 "Imm, the
flattest of the entire series. Steps were conspicuous, occurring about every 120 p. In
contrast, penetration 4 (fig. 4C), which
made an angle of 46" to the surface, had a
slope of 273"lmm and the orientation
changed with each 2 5 3 0 p advance of the
electrode, i.e., too frequently for individual
steps to be resolved. The interruption in
this penetration between 1.8 and 2.5 mm
marks the passage of the electrode through
layer IV C, where as usual there was no
hint of any orientation specificity and responses were strictly monocular (Hubel and
Wiesel, '68). Following this interruption
the curve showed about the same slope as
before, and appeared to represent a simple
continuation of the sequence. This is what
is expected if the columns extend through
the full thickness of cortex.
A second example comparing oblique
and nearly perpendicular penetrations is
shown in figure 5. After crossing the outermost thickness of cortex and white matter
beneath, the electrode entered the mushroom-shaped calcarine cortex, where it
pierced one fold completely, at 82" to the
surface, and finally entered the next fold
at 51 '. In the first of these calcarine folds
the receptive fields were 12 from the fovea,
in the second, 18". Once again the more
O
.
IVr
1 rnm
Fig. 4 A Reconstructions of two penetrations in
the right striate cortex. P3 was almost normal to
the surface, whereas P4 made an angle of 46' with
it. Fields were 1 below and 1 to the left of the
fovea. (Experiment No. 10.)
perpendicular traverse gave a relatively flat
curve ( - 106"Imm), whereas for the oblique
portion the curve was much steeper (283"/
mm). (It is not clear why discrete steps
did not occur in the first curve.)
A third comparison between perpendicular and oblique penetrations is shown below in figure 13, for the cat.
That the three perpendicular penetrations in these examples gave very flat curves
agrees with our previous experience (Hubel
and Wiesel, '62, '68), and is in marked contrast with the relatively steep slopes observed for the straight segments of the
curves in virtually every oblique or tangential penetration in the series.
Dimensions of orientation columns
A summary of the information obtained
from all the penetrations of the series is
given in table 1. Our purpose here is chiefly to convey a n overall impression of the
degree of variability of the results. The
mean value for the total orientation shift
in 1 mm of tangential component of the
electrode movement ("slope corrected") is
281"lmm. As already mentioned, the distribution of the slopes favored high values,
with only one slope less than 100"/mm. The
mean slope of 281 "/mm, corresponds to
640 p for a full sweep through 180", a value that is likely to be a somewhat high estimate of the thickness of a full 180" complement of orientation slabs since, as
mentioned above, we have no way of knowing in single penetrations the angle between
the slabs and the horizontal component of
h
0,
275
ORIENTATION COLUMNS IN MONKEY STRIATE CORTEX
' Ol
Fig. 4B Graph of orientation vs. track distance for the perpendicular penetration P3. Slope
-54"/mm, uncorrected for angle to surface. The filled dark bar represents activity in layer IV
C, which was influenced exclusively from the ipsilateral eye and showed no orientation selectivity; the bar's placement along the orientation axis is arbitrary.
-
90,
1
60,
/
30,
I
... ....'
..
0,
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-30,
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0
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60,
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30,
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60,
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90
0.
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8
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1
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2 76
DAVID H. HUREL AND TORSTEN N . WIESEL
Fig. 5 A Comparison of perpendicular and oblique penetrations. Reconstruction of a penetration that passed through two folds of striate cortex deep in the calcarine fissure. Field positions 1 2 O and 18' from the fovea; parasagittal section, 1 0 mm to right of midline. Parts of track
indicated by continuous line are plotted in figure 5 B . Electrode intersected the first calcarine fold
at 82O, and the second at 51'. Monkey had a n artificial strabismus from birth. (Experiment
No. 3 . )
I
OI
2
\
-30-
\
-60-
-
90-
/
60-
/
30-
I
0-
4
5&
+
..
\ -30\
-60-
-
90-
/
60-
/
30-
0
00
0"
I
0-
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-60-
o.>3
0's
7'0
0
75
810
TRACK
8'5
9'0
$5
10'0
10'5
DISTANCE - m m
Fig. 5 B Orientation vs. track distance, for the portion of penetration indicated by a continu o u s line, in figure 5 A . Open circles, contralateral eye; closed circles, ipsilateral eye. Slopes,
- 106"/mm, 283'1mm.
12
9
1
4
3
7
2
1
2
1
2
1
2
3
4
1
1
2
1
2
1
2
1
2
1
1
1
2
Cat
macaque
area 18
macaque
squint
macaque
normal
macaque
normal
macaque
normal
macaque
normal
macque
normal
macaque
normal
1
2
2
1
2
10.5
10
2
2
1
7.5
3
3
0
1
2
-15
- 4.5
- 4.5
- 4.5
- 4
- 4.5
- 4.5
- 5.5
- 1
-
- 4.5
- 3
3.5
i.yrees j
-
(d
2.25
5
5
12
18
5
5
5
4
1.5
6
7.5
5.5
4
3.5
130
159
146
215
61
282
42
323
271
204
174
188
267
157
131
83
97
191
59
224
152
145
107
52
134
291
61
489
149
175
89
60
180
([leg
deg.
40
31
29
25
25
20
20
20
12
31
31
7
7
58
25
25
17
17
(90)
46
46
42
32
(82)
51
19
19
39
67
45
38
(90)
3
mm
1.01
0.50
0.78
0.84
0.29
1.22
0.28
1.27
1.24
0.59
0.62
0.73
0.82
1.68
0.48
0.82
0.37
0.87
1.07
0 90
0.85
0.56
0.54
0.58
0.43
1.41
0.36
2.06
1.1
0.9
0.64
1.07
1.24
1.24
-
0.27
133
0.34
1.60
0.41
0.64
0.50
-
0.63
0.59
0.42
0.46
-
mm.
0.77
0.43
0.68
0.76
0.26
1.15
0.26
1.19
1.21
0.51
0.53
0.72
0.81
0.89
0.44
0.74
0.35
0.83
-165
28 1
93
8.
-
451
231
231
281
363
-274
-176
-
408
378
430
-288
222
83
-
-201
-358
-202
-221
250
-232
164
-280
208
424
358
265
421
121
290
124
297
237
"/mm.
-154
-307
-177
-200
226
-218
154
-262
204
363
307
263
417
64
263
112
284
227
- 54
283
263
320
-244
-106
283
219
219
219
142
-194
-139
54
-165
'lrnm.
11
9
9
14
17
-
27
7
7
9
10
-
13
15
11
12
23
9
21
13
26
16
11
13
19
8
31
7
28
24
14
15
17
11.91
3.4
13.5
19.4
9.9
4.3
10.6
-
5.8
19.1
10.7
8.7
-
8.1
14.5
11.2
8.0
7.6
9.1
6.0
11.5
11.3
14.6
11.6
11.1
10.3
12.1
8.7
7.6
8.1
8.3
10.7
11.7
14.5
deg.
43.26
11.5
73
-
37
70
55
-
39
49
49
-
-
30
45
42
-
48
39
52
40
33
37
37
43
50
36
35
42
31
68
29
67
29
36
fim
13b
13c
12
12
5B
5B
7B
4B
4c
4c
2
8B
8B
3,8C
3,8C
1,8D
10
10
10
2
6
'
1 "Sequence" refers to a group of orientation shifts all In o n e duection. FlgHorizontal track length = track length X cos 8..prnt, pvnc.
" V e r y roughly, this is given by span - track length, usually computed
urv SD ( c x p t . 5 . penrtrntion 3 ) cniitiiiii\ o n
from graphs. 177.2/tan (an le o f curve to orientation a x i s ) .
tr.ition 1 J c ~ i i t a i n stwo m;uor and two iuntabu
9 Uncorrected slope/cos
2 Horizontal component of distance from fovea.
I t ' Span/(no. of shifts).
3 Vertical component, positive values upward.
Distancr from fovea.
Horizontal track lengthi(no. of shifts).
5 Lpngth of the sequence In degrees.
Means for all normal and abnormal macaqne area 17 ( a l l of table 1 exAngle between electrode track and cortical sUrf:lCr 1 M E T H O D S )
cept experiments 2 and 8).
Means
s.d.
8
2
1
3
2
3
4
3
1
2
3
1
2
3
1
10
9
7
6
5
2
2
2
3
1
1
1
1
~
4
~~
TABLE 1
4
4
IG
x
m
0
0
P
ei
M
ei
>
2E
4
x
m
8z
2
z,
2
0
0
=!
z
5>
Em
0
2 78
DAVID H . HUBEL AND TORSTEN N . WI ES EL
the electrode tracks. The mean value for
“horizontal distancelshift” of 43 p is also
probably a high estimate for slab width,
partly for the same reason, and partly because it is likely that some orientation
shifts went unobserved. The same applies
to the mean value for “anglelshift” of
11.9”, as an estimate of the angular shift
between slabs.
A closer approach to the true values of
these items can probably be obtained from
the penetrations that gave the most frequent intervals, with the smallest shifts in
angle. The sequence shown in figure 1, for
example, gives a mean value for “horizontal distancelshift” of 25 p and a mean
“anglelshift” of 7.2 ; the comparable numbers from the second sequence of figure 2
(experiment no. 7) are 31 p and 10.3”. In
the present study one objective was to obtain some rough estimate of column size.
As a summary statement it seems reasonable to say that the columns are 25-50 p
wide and are arranged in sequences of
9-10’ steps. Both of these figures are upper
limits and obviously would be meaningless
if orientation were a continuous function
of horizontal distance, in the statistical
sense discussed below ( D I S C U S S I O N ) . In either case, an array of columns subserving
a full 180” has a total width of 0.5-1 mm.
Systematic shifts in orientation were
seen in all layers of the cortex with the exception of layer 1, where no responses were
generally seen, and IV C, in which responses were not orientation specific. There
were otherwise no obvious differences from
layer to layer in the shapes of the curves,
the size of the orientation shifts, or slab
thickness. Most of the recordings were
made from layers I1 and 111, however, and
with such a limited survey one cannot rule
out the existence of subtle differences between layers.
O
Variation of c o l u m n s size w i t h
eccentricity
Most of our experiments were done in
cortical areas representing visual fields
5-10” from the foveal representation (table
1), in order to form some idea of the range
of variation of the columns in at least one
region. One pair of penetrations, however,
was made in the foveal representation (fig.
4) and another went beyond the exposed
surface of area 17 into the calcarine fissure
where it intersected the cortex twice (fig.
5), with receptive-field positions 12” and
18” from the fovea. As expected, in the
fovea the fields and the random variation
in field position (“scatter”) were both very
much smaller than what was found 5-10”
out, and these in turn were smaller than
the fields and scatter 12-18’ out. In contrast, there was no indication that the column size varied with eccentricity: the
slopes of the graphs of orientation vs. track
length, the frequency of occurrence of
shifts and their angular size, and the frequency of changes in ocular-dominance
were all similar (table 1).
T o be certain that the columnar organization is uniform in all respects over the
entire cortex would of course require a
much more extensive survey. One can,
however, be confident that there are no
gross differences between center and periphery such as exist in magnification factor or receptive-field size. From the curve
of Daniel and Whitteridge (’61, fig. 4) the
magnification factors corresponding to
fovea and to points 7 ” and 15” from the
fovea are roughly 6.3, 1.3 and 0.4 mm/”.
Had the orientation columns differed in
size in these proportions (16:3:1) it should
have been evident. Our conclusion concerning the ocular-dominance columns (Hubel
and Wiesel, ’72), based on anatomical
methods, was similar: there is no very
striking change in the widths of the stripes
with eccentricity.
Relationship b e t w e e n ocular-dominance
and orientation c o l u m n s
Physiological and anatomical studies in
the macaque monkey indicate that the
width of ocular-dominance columns is in
the order of 0.25-0.5 mm (Hubel and Wiesel, ’68, ’72). In an average tangential
penetration one should therefore expect to
see many shifts in receptive-field orientation for each shift in eye dominance. The
relation between the two types of column
can be illustrated in several typical penetrations. In the example shown in figure 6,
from a normal monkey, cells in the first 0.5
mm of the penetration were driven almost
exclusively from the ipsilateral eye. Then,
for about 0 . 3 mm, the cells were roughly
equally influenced from the two eyes. Finally, in the last 0.2 mm, the contralateral
eye had complete control. All this time
ORIENTATION COLUMNS IN MONKEY STRIATE CORTEX
279
etration, before entering layer IV, was the
closest approach of any to a straight line
(coefficient of linear correlation 0.996),
and the line was again virtually uninterrupted by the transition from ipsilateral to
contralateral eye. (The slight apparent
shift in the curve is explained by a relative
outward rotation of the eyes in the equatorial plane.) During the 2 mm long passage through layer IV C, marked by arrows
in the reconstruction, there were three
ocular-dominance shifts, and a final shift
'
'
O 1
...
-"i
6
0'2
1
L,
0'4
TRACK
0!6
DISTANCE
0'8
- mm
1'0
1'2
Fig. 7A Relation oforientation shifts tochanges
in ocular-dominance. Reconstruction of a penetration in the same monkey as in figure 5 (strabismic), but at a slightly smaller angle to the surface
( 1 9 O ) and 200 /L lateral. Region of penetration in
which responses lacked orientation specificity is
marked with arrows. This coincides closely with
layer IV C. (Experiment No: 3.)
Fig. 6 Relation of orientation shifts to changes
in ocular-cominance, in crossing from one oculardominance column to another. Graph of orientation vs. track distance, for a penetration that entered striate cortex in the parasagittal plane 10 m m
from the midline, making an angle of 40° to the
surface. Normal monkey. Most of the first cells
were strongly dominated by the ipsilateral eye
(closed circles), but after the electrode passed
through a region of mixed dominance between 0.6
and 0.9 mm, it entered a region of contralateral eye
dominance (open circles). (Experiment No. 4.)
the orientation progressed steadily in a
counterclockwise direction, at virtually the
same rate for all parts of the penetration
regardless of eye dominance.
In the strabismic animal the results were
similar except that transitions from one eye
to the other were abrupt, with, at most,
only very short spans in which both eyes
were represented. An example of this has
already been seen in figure 5, and another
example from a different penetration in the
same experiment (No. 3 ) is shown in figure
7. The curve from the first part of this pen-
..
Fig. 7B Graph of orientation vs. track distance.
Closed circles, ipsilateral eye; open circles, contralateral. The relative counterclockwise displacement
of the graph at the point of transition from one eye
to the other near the beginning of the penetration
was caused by a relative extortion of the two eyes.
280
DAVID H. HUBEL AND TORSTEN N . WIESEL
Fig. 8 A Reconstruction of three closely spaced penetrations ( P I - PB)in right striate cortex.
Each penetration was in the parasagittal plane, with PI most medial, Pz 200 p lateral to It,
and P:, 200 p lateral to P p . In the reconstruction, the three are seen in profile, as though they
were in the same parasagittal plane. A l l three penetrations were restricted to layers 1-111.
(Experiment No. 5 )
tions were made 0.2 mm apart in a normal
monkey. Three tracks intersected the surface of the cortex at angles of 25 O , 20 and
20". The pattern of shifts in each of the
three penetrations was highly regular, and
the slopes of the three graphs were reasonably similar, with values, corrected for inReconstruction of closely-spuced
clination to the surface, of -221, -232.
penetrntzons
and -280"Imm. It is difficult to control
I t should be possible to test the idea that the exact point of entry in a penetration
orientation columns are parallel slabs by that is close to tangential, and penetration
making several parallel penetrations 1 overlapped the other two for only about
through a small region of cortex, compar- one-half of its length.
ing receptive-field orientations of adjacent
A reconstruction of these penetrations
points. In practice this proved difficult. from the histology is shown in figure 9. To
In our first attempt, two parallel penetra- the left in the figure the three penetrations
tions were made 1 mm apart, and though are viewed from above, as though projected
both sequences were regular the rotation onto the plane of the cortical surface; in
was clockwise in the first and counterclock- the right half of the figure they are viewed
wise in the second. This result is perhaps from the side as in figure 8 A . On comparnot surprising, considering how abruptly a ing the receptive-field orientations in neighsequence can go from clockwise to coun- boring tracks one can imagine the slab
terclockwise or back in a single penetra- walls running in roughly the directions intion, but if one is to understand the geom- dicated by the thin continuous lines. These
etry of the columns a closer spacing of lines are drawn every 45" except in one
penetrations is clearly required.
place where they are spaced at 9 " to give
Figure 8 illustrates the results of a n ex- an indication of the probable upper limit
periment (No. 5) in which three penetra- of the column thickness. The lines repreoccurred in the traverse through layer V .
These results, in summary, indicate that
sequences of orientation shifts are undisturbed by ocular dominance; to this extent
the two column systems are certainly independent.
ORIENTATION COLUMNS IN MONKEY STRIATE CORTEX
28 1
'11
' I
'
OT8
8
.
I;,
ill
0'6
"i
1'0
1'2
TRA-IX
D,ST*Nit
" 6 1 ' 8 -
$4
~
7%
2'2
ll,"
Fig. 8B Orientation vs. track distance of P,.
T h e gap beginning at about 0.95 mm is caused by
the first lesion (L,). Activity at the outset was dominated by the left eye (contralateral, open circles),
but the dominance soon switched to the ipsilateral
eye, and finally it switched back again to the contralateral at 1.5 mm. Angle to surface, 25". Slope
of the first, descending, sequence, -200"/mm uncorrected, -221 "Imm corrected, for the inclination of the electrode.
...
Fig. 8C Graph for Ps,of orientation vs. track
distance. Electrode inclination 20"; slope of the
main sequence, uncorrected for inclination, -218"/
m m ; corrected, - 232"lmm. For description of the
breaks in the sequence at 0.3 mm and 0.6 mm,
see text and figure 3.
senting the tracks are shown as continuous
in regions of ipsilateral-eye domination,
and interrupted where the contralateral
eye dominated. While there is too little territory mapped to do more than suggest
roughly the form of the ocular-dominance
columns (dotted lines), one can at least get
- ,
,
,
,
t
L,
j--T
-~
o"
tT
l-5
-,
,en<I( Dlili.NCt
I.,
..I,,,
Fig 8D Orientation vs. track distance for Po.
Electrode Inclination 20°. Slope -262"Imm uncorrected, --- 280Vmm corrected, for inclination.
some idea of their size relative to that of
the orientation columns.
The abrupt breaks in penetration 2 (fig.
8C) have already been discussed above
(fig. 3 ) . Curiously, just at the second discontinuity the cells responded to specifically
oriented red slits but not to white stimuli
of any kind. We have previously observed
that color-coded cells in the monkey striate
cortex tend to be aggregated in small
groups (Hubel and Wiesel, 'SS),but whether or not these are columnar is not known.
That such a group occurred here together
with discontinuities in the main orientation
sequence is interesting, and perhaps not
entirely coincidental since it may be that
groups of colorcoded cells are interjected
as separate islands with separate sequences
of orientation, in an otherwise well-ordered
matrix of columns. No colorcoded cells or
abrupt jumps were seen in the other two
penetrations, but in the reconstruction
the clockwise sequence of penetration 2 is
physically very close to the similar clockwise progression at the end of penetration
1, and is probably related to it.
A second set of parallel penetrations in a
normal monkey is illustrated in figure 10
and reconstructed in figure 11. Here the
lateral spacing between penetrations was
282
DAVID H . HUBEL AND TORSTEN N . WIESEL
p1 p2 p3
ant.
I
I
I
I
.
I
-.-*....
lat.
.....
/
6
post.
r
I
1 mm
Fig. 9 Reconstruction of the three penetrations of figure 8. To the right of the figure the tracks are
seen from the side, as in figure 8A. To the left, the three penetrations are seen a s though the cortex
were viewed from above. Each penetration is drawn a s a vertical line, continuous for regions of contralateral-eye dominance, interrupted for ipsilaterd. Black dots indicate polnts where the penetrations
began: in P3 no activity was recorded for roughly the first 1 mm. Dotted lines are intended to suggest
boundaries between ocular-dominance columns. Continuous thin lines indicate boundaries of orientation columns, spaced at 4 5 O except near L,, where spacing is 9' to give a rough impression of the
size of the individual orientation columns.
283
-
\ -30
-
,-60
-
90.
.
0
.
/
60-
-.
..
.=.. ..
/ 30-
I
. ..
..
0-
-30,
..
\-60-
-
900
0
Z
0
0
..
60-
.
.
.
IlO
0!5
0
60-
/
30-
I
0-
oo
115
0 0
0
2'0
60-
.. -
/ 30-
I
...
\ -30-
..
0
0-
.
..
\-30-
,
-60 -
,-60-
-
- 90-
90-
.'
.*:
/
..
60-
L2
0'2
0'4
0'6
0'8
i
lb
TRACK
'60-
**
0'6
0'4
DISTANCE
-
0'8
Ib
mrn
Fig. 10 Graphs of orientatlon vs. track distance for three parallel penetratlons in parasagittal planes 100 p apart. (The three reconstructions are seen in profile and plan views in fig.
11.) Slopes, uncorrected and corrected for electrode inclination, P I , 204,208; P p , 363,424;Pa,
307, 358 - all in "Imm. PI entered the cortex behind the other two, so that the total extent of
cortex explored was about 2.2 mm, throughout which the trend of orientations was clockwise,
going posteriorly. (Experiment No. 6.)
284
DAVID H. HUBEL AND TORSTEN N . WlESEL
p1 p2 p3
ant.
med.
Fig. 1 1 Reconstruction of three parasagittal penetrations 100 K M apart, whose graphs of
orientation vs. track distance appear in figure 10. Side view is shown in the right part of the
figure; surface view on the left. The large dots indicate points of entry of electrode into cortex;
in P2 and P3no responses were recorded for the first 0.5-0.75mm.
285
ORIENTATION COLUMNS I F MONKEY STRIATE CORTEX
0.1 mm; again one of the penetrations entered some distance beyond the others so
that there was no overlap with them. The
slopes of all three penetrations were again
very similar, and the reconstruction of penetrations 2 and 3 are once more consistent
with the idea that the columns are parallel
slabs.
Area 18
In one monkey six penetrations were
mad.- in area 18 and 111 shifts in orienta-
Fig. 12A Penetration in monkey area 18. Electrode entered the cortex in the parasagittal plane
,just anterior to the 17-18 border.
tion were observed. One penetration in
which 44 cells were recorded is illustrated
in figure 12. The animal had had one eye
removed at birth for a different study, so
that variation in ocular-dominance could
obviously not be examined. Although six
penetrations are far from enough to allow
a n y close comparisons between areas 17
and 18, it is clear that in area 18 orientation columns are present and are systematically arranged, with similar long
sequences of orientation shifts broken occasionally by reversals. A similar orderliness in arrangement of orientation columns
in area 18 was previously observed in the
cat (Hubel and Wiesel, '65, fig. 32). The
fineness of orientational representation
and the size of the columns seem not to
differ very greatly in area 17 and 18.
Recordings f r o m cut
Four penetrations were made in the striate cortex of one cat. Systematic variations
in orientation were seen in all four penetrations, two of which are described in figure 13. Penetration 1 was almost perpendicular to the cortical surface, and penetration 4 in its latter part was almost parallel.
A s in the monkey, the slope of the graph
..
..
-
901
. .
*
..
.
.
.
. .
I
1
10
3 '0
20
TRACK
DISTANCE
-
rnrn
Fig. 12B T h e graph of orientation vs. track distance shows that orientation varied systematically with position. This animal, from a separate study, had had its right eye removed from
birth, so that nothing can be said about eye dominance. (Experiment No. 2.)
410
286
DAVID H. HUBEL AND TORSTEN N. WIESEL
left
Fig. 1 3 A Cat striate cortex. Reconstruction, in the coronal plane, of two penetrations in the
postlateral gyrus, roughly at Horsley-Clark P 2.0. Penetration in right hemisphere was virtually
perpendicular to the layers throughout. On the left side the electrode passed through the dorsal
thickness of grey matter, and then through white matter, finally re-entering the mesial segment
of striate cortex, intersecting the radial fascicles at about 87". (Experiment No. 8.)
of Orientation vs. track distance was much
less for the perpendicular penetration.
In comparing cat and monkey one major
difference suggested by figure 13 is in the
size of the orientation columns. In the tangential penetration (P. 4, fig. 13C) steps
were evident, whereas in the monkey, as
already mentioned, the steps were usually too small to be resolved by our methods
except in nearly perpendicular penetrations. The horizontal distance/orientation
shift for this penetration was 73 f i , compared with a mean of 43 ,.L in the monkey.
The column thickness suggested by SINface mapping techniques in our previous
work in the cat was about 100 ,.L (Hubel
and Wiesel, '63, fig. 4).
The histological sections in the region
of this tangential penetration were especially favorable for comparing numbers of
radial bands of cells with the steps seen
physiologically, since the point of entry
into cortex from white matter was clearly
marked by the track, and the end of the
track by a lesion. We counted roughly 35
bands along this track (23 banddmm, i.e.,
average width of band 43 p ) whereas the
number of observed shifts was 17 (14/mm,
average distance between shifts 73 p ) . A s
in the monkey, the two seem to be about the
same order of magnitude, the number of
banddmm again being somewhat larger
than the number of shifts.
DISCUSSION
The column concept
The results of this paper indicate that
orientation columns are highly ordered and
probably have the form of parallel slabs.
This seems to be true in the cat as well as
in the monkey and in area 18 as well a s in
area 17. That stimulus orientation turned
out to be so systematically related to position along the cortical surface was not entirely a surprise, since we had observed a
compelling example of it before (Hubel
and Wiesel, '68). Until the present study,
however, with the use of lower impedance
electrodes and the plotting of orientation
against distance, we had not realized that
the orderliness is the rule rather than the
exception. Since such a highly patterned
machinery must surely have some important biological significance, i t may be useful to think through once more the concept
of the cortical column before discussing the
implications of the orderliness.
The cortical column may generally be
looked upon as arising from the necessity to
portray more than two variables upon a
287
ORIENTATION COLUMNS IN MONKEY STRIATE CORTEX
/
0
F-
\
301
-30
6
+
z
y1
\-60
8
-
RIGHT
I
90i
...
..*
I
' 60-
.....'* ....
.-•
.. .....
. . ..
3
.*
.
0
- 0
L1
I
I
I
Fig. 1 3 B Graph of orientation vs. track distance for the perpendicular penetration in the
right hemisphere. Slope, uncorrected. 54"/mm.
/
I
30
LEFT
0 I
0
000
-30
\
0000
.........
0 . .
I
01
...
.......
/
60
30
.
..
0 . .
I 0
2.5
3.0
TRACK
DISTANCE
3.5
-
...
..
..
4.0
mrn
Fig. 13C Graph of orientation vs. track distance for the part of the penetration in the left
hemisphere indicated by a continuous line. Slope, corrected for the 3" inclination, - 165"lmm.
i
288
DAVID H . H U B E L AND TORSTEN N. WIESEL
two-dimensional surface. The two surface
coordinates are used up by the topographic
representation of the visual fields, and
it is the engrafting upon this representation of two more variables in the form
of receptive-field orientation and ocular
dominance that leads to the two sets of
subdivisions. It is important here to emphasize the hierarchy: the topographic projection is the primary one, and for
each position in the visual field there is
a machinery €or each orientation and €or
each eye. How the topographic representation and the two columnar systems interrelate, in detail, is taken up in a later
paper (Hubel and Wiesel, ’74a).
That we speak of the cortex as a twodimensional structure in this context is
deliberate, for the three variables, visualfield position, orientation, and ocular dominance, all remain virtually constant during
a perfectly perpendicular penetration. The
cortical depth dimension is apparently concerned with other problems, such as the
relative complexity of cells and their hierarchical order. For a columnar system,
then, a prime criterion is that there be subdivisions extending vertically through the
full cortical thickness, with walls perpendicular to the surface and to the layers.
This is fulfilled by the ocular-dominance
columns, as we know from both anatomical
and physiological evidence. For the orientation columns previous evidence (Hubel
and Wiesel, ’62, ’63) has been reinforced,
in the present paper, by comparing slopes
of orientation-vs.-distance curves in perpendicular penetrations with those obtained
in tangential or oblique ones.
The requirement that the walls of the
columnar subdivisions be perpendicular to
the surface and to the layers predicts a
cylindrical shape (or a conical shape, if the
cortical surface is curved). Since “cylinder” summons up visions of highball glasses, coins, or Greek pillars, the word “column” originally seemed a natural choice.
In the somatosensory system, where the
term was first used by Mountcastle (’57),
the geometry is still unclear, but in the
two column systems so far described for
the visual cortex the cylinders seem to take
the extreme form of a set of sheets, a shape
that does not come to mind on hearing the
word “column.” We retain the term partly
for historical reasons and partly because
it has become associated, in cortical physiology, as much with the principle of grouping of cells with certain physiological
similarities, as with any special shape. Furthermore, before considering a change in
terminology, it is well to note that even in
the ocular-dominance system, where by
anatomical methods we have obtained some
inkling of the surface mosaic, the form
seems to be one of stripes only to a f i s t
approximation: in some experiments the
stripes seemed to subdivide and rejoin or to
be crossconnected, occasionally to such an
extent that the geometry resembled an
interlacing kind of lattice rather than parallel plates (Hubel and Wiesel, ’72, fig.
17).
An additional requirement that has
usually been insisted upon for a columnar
system is that the subdivisions be discrete.
This means that within a certain finite volume of cortex the variable concerned must
remain constant. The ocular-dominance
columns are certainly discrete, and hence
properly named. With the orientation columns, on the other hand, the situation is
less clear, especially in view of the present
results. In tangential or oblique penetrations in the monkey any discrete steps were
too small to be resolved, since every clearcut advance of the electrode was accompanied by an orientation shift. The only
exceptions to this a r e the relatively infrequent but nevertheless very clear large
shifts such as the two illustrated in figure
3 ; in cases like these there can be no doubt
that the change in orientation with movement parallel to the surface was abrupt
and discrete. Otherwise the notion that the
orientation shifts are discrete relies, in the
monkey, upon a very few penetrations that
were virtually perpendicular to the surface,
in which the distance from slab to slab
was presumably magnified, and in which
the curves showed clear steps (fig. 4B). In
the cat cortex, where the columns are probably thicker, steps were apparent even in a
penetration parallel to the surface (fig.
13C), so that here the existence of discrete
orientation columns seems reasonably
clear.
Though it is conceivable that orientation may vary continuously with movement
along the cortex, there are certain difficulties in the idea. Taken literally, it is contradicted by the fact that the cells which
ORIENTATION COLUMNS I N MONKEY STRIATE CORTEX
make up the cortex and from which one
records are discrete entities. A kind of continuous variation might nevertheless be
achieved if there were a small random
variation in the orientations of neighboring cells, and if accompanying horizontal
movement through the cortex there were
superimposed a steady drift or progression
in the orientation. This would be analogous
to the random variation or staggering in
receptive-field positions of neighboring cells,
upon which is superimposed a steady drift
in receptive-field position with movement
parallel to the surface. We did not, however, observe a n y such random variations
in orientation, from one cell to the next.
Variations comparable to those seen in receptive-field position would have produced
jagged curves, not the smooth monotonic
ones found in this study. Moreover the
multiunit background activity showed an
orientation preference that was generally
the same as that of simultaneously recorded cells, and no less sharply tuned. There
is thus no evidence to support the existence
of a local random variation in orientation,
but at present this possibility cannot be
ruled out conclusively.
To recapitulate, the orientation slabs in
the monkey, if discrete entities, are so thin
that they cannot be clearly resolved in tangential penetrations, because of imprecision in measurements both of electrode distance and receptive-field orientation. The
evidence favoring discrete entities comes
from perpendicular penetrations, from the
occasional abrupt discontinuities seen in
tangential penetrations, and from results
in the cat, where the columns are coarse
enough to be resolved. The alternative notion, that substantial regions of visual cortex are organized with respect to the orientation variable in some kind of continuous
manner, cannot be ruled out, though it
seems rather less likely. Independent of
which alternative is correct, the central
concept of a subdivision of cortex into regions of common orientation specificity by
surfaces arranged perpendicular to the cortical layers still holds. If the slabs are not
discrete it obviously becomes incorrect to
speak of steps of 9-10" or slabs 25-50 p
thick, but the notion of 180" being covered
in 0 . 5 1 mm movement normal to the smfaces is still valid.
If one accepts the notion that the orien-
289
tation columns are discrete, with an interval of roughly 9-10', does this mean that
orientation over the entire 180" is quantized into 18-20 strictly defined groups in
terms of angle? If, beginning at a certain
point on the cortex, corresponding to a certain optimal stimulus orientation, one proceeds along the surface from orientation
to orientation until a full cycle of 180" has
taken place, will one have returned to precisely the same orientation, or will it be
slightly different? At present we have no
way of knowing the answer to this, and
given the breadth of the tuning curves and
the limitations in precision of measurement, it is not likely that an answer will be
easily found. Intuitively the idea of strict
quantization seems somewhat unattractive,
since to develop such a system would probably be more difficult, with no obvious
advantages over the fuzzier alternative.
To summarize: the column is usually defined as a discrete aggregate of cells whose
shape is that of a sheet, or more generally
a cylinder, with walls perpendicular to the
surface. The physiological variable that defines a set of columns is represented by
being engrafted upon a pre-existing twodimensional mapping. Although field position in the cortex remains constant (aside
from a random scatter) along the depth
axis, this by itself does not result in a columnar system unless one is willing to see
the concept of the column degraded, since
there are no discrete aggregates, and since
the topography itself forms the system upon
which columns are engrafted. Similarly
the projection-line system of topographic
representation in the lateral geniculate
body (Bishop et al., '62) should not be regarded a s columnar. The mouse cortical
whisker barrels are certainly discrete (Woolsey and Van der Loos, '70), but they constitute a topographic representation rather
than being superimposed on one. Whether
they should be considered columns seems a
matter of taste and semantics. The orientation columns, finally, if discrete, certainly
fall within the definition of the term column. If orientation varies continuously
with distance there are again semantic difficulties - either one must broaden the
definition of the column or decide that the
system is not strictly columnar. In fact,
however, the distinction may be somewhat
academic, since if the columns are discrete
290
DAVID H. H U B E L A N D TORSTEN N. WIESEL
penetrations gave relatively steep curves.
Since most penetrations were made in the
parasagittal plane, one wonders if the slab
Geometry of orientation columns
orientation is constant, from animal to aniEver since our finding with silver-degen- mal, running perpendicular to the paraeration techniques that ocular-dominance sagittal plane, i.e., parallel to the 17-18
columns are to a first approximation slab border behind the lunate sulcus. This
shaped, we have hoped to fipd a similar seemed only a remote possibility until remethod for revealing the shape of the orien- cently, with the finding that the oculartation columns. None has yet been forth- dominance columns do in fact have a concoming, though direct physiological evi- sistent pattern from animal to animal,
dence for a slab shape was obtained by intersecting the 17-18 border a t right anmaking multiple superficial penetrations gles (LeVay et al., '75). A s mentioned bein the cat (Hubel and Wiesel, '63),and by low, it is theoretically attractive to suppose
reconstructions of parallel penetrations in that the two sets of slabs, if they have a n y
the present study. To obtain a more exact constant relationship, intersect each other
idea of the shape of the slabs will require at right angles.
It turns out, however, from simple trigmore studies using multiple penetrations
but meanwhile we are given a much better onometry, that a parameter such as the
insight into the geometry of the columns by slope of these curves is very little affected
the observation that their arrangement is by the angle of intersection of a horizontal
highly regular. The slab shape, in fact, track with the slabs, until that angle beseems a n inescapable consequence of the comes very small. As an example (fig. 14),
regularity. Suppose that whenever a n electrode moves tangentially through the cortex
I
it records either small regular orientation
shifts or no shifts at all. Then a three-dimensional graph of orientation (as the Zaxis) against cortical position (X- and Yaxes) will give a smooth surface, or strictly
spealung one terraced in %lo" steps.
Each of the curves of orientation vs. track
distance simply represents the intersection
of this surface with a plane perpendicular
to the X-Y plane and passing through the
electrode track. On such a surface the contour lines of constant orientation represent
the column mosaic as it appears when the
cortex is viewed face-on. These contour
I
I
05
10
lines define the tops of the slabs. Thus withTRACK DISTANCE out appealing to rigorous arguments inFig. 14 Theoretical effects of varying the angle
volving topology or mathematical theories between a set of parallel orientation slabs and a tanof continuity it seems intuitively obvious gential electrode, upon curves of orientation vs.
that the absence of breaks in regularity track distance. The uppermost curve corresponds
implies a set of slabs. These may be straight to a head-on 90" intersection of the electrode and
the slabs; a slope of 40O0/mm w a s arbitrarily selector curved depending on the shape of the ed for the example because the steepest experimensurface in the three-dimensional graph.
tal curves were in the range of 4 0 0 4 5 0 ° / m m . A s
If the columns indeed have the form of the angle between the electrode and the slabs varslabs, one may predict that in tangential ies, the slope falls according to the sine of the
angle, with littlechange u p to about 40-SO", giving
penetrations some of the tracks should curves that a r r f a r from flat even a t ZOO. Thus if
thread their way - . ' o I , ~the plane of the tangential penetrations intersect the slabs at ranslabs, producing a flat or nearly flat graph dom angles there should be a skew distribution of
of orientation vs. track distance just a s was slopes, with a preponderance of steep curves. If
the slabs are parallel but curved, reversals in direcobtained with penetrations perpendicular tion of rotation from clockwise to counterclockwise
to the surface. In this study most tangential or back should be abrupt.
their thickness is close to the size of a single cell body.
mm
O R I E N T A T I O N C O L U M N S I N MONKEY STRIATE CORTEX
suppose that a n electrode intersecting the
slabs at right angles were to give a curve
of slope 400"/mm. How is the steepness of
the curve affected for approaches different
from go"? The calculations show that the
change in slope for angles up to about 50"
is slight (the slope is 400 sin 50", or 306"/
mm), and even at 20" the curves are hardly what would be called flat (137"/mm).
The same applies to variations in the angle
between the electrode and the surface of
the cortex, and indeed curves as flat as
those of figures 4B, 5B (first part) and 13B
were obtained only in penetrations that
were within a few degrees of perpendicular. Thus in tangential penetrations, at
what are presumably random angles with
respect to the slabs (since we do not have
a n y idea of the slab orientations), the
slopes cannot be expected to be distributed
evenly between some maximum value, such
as 400"/mm, and zero. In fact the slopes
we obtained (table 1) were not so distributed but were, a s would be predicted,
skewed markedly towards higher values.
One curious property of the orientation
columns, illustrated in figures 2A and 8B,
is the reversal of the sequences from clockwise to counterclockwise and back between
uninterrupted spans of the order of 270360". Only more ambitious mapping will
help in understanding the origin of these
reversals. Possibly the columns are virtually straight parallel slabs, and the order
may simply reverse at irregular intervals.
This would mean that the surface generated by plotting orientation against position on the cortical surface would be corrugated like the bellows of a camera. The
abruptness of the reversals might seem to
argue for this: the curves of orientation vs.
track distance are not at all sinusoidal, but
the sequences progress with remarkable
linearity and reverse not by gradual flattening but fairly suddenly. A second possibility,
however, is that the slabs, viewed from
above, are not straight but form whorls,
in which case the surface would consist of
mountains and valleys. If that were so, a
straight electrode track would constantly
change its angle to the slabs, and would be
expected at times to become tangential
and then to reverse its direction through
them. One might expect, on first thought,
that this would give curves with gradually
291
changing slopes, but as pointed out above
the slopes of the graphs are not greatly
affected until the approach becomes almost tangential. The result of this would
be to increase the abruptness of the reversals. The information from reconstructions
of parallel penetrations is so far too fragmentary to allow us to choose between
these possibilities, but presumably more
extensive mapping can settle the question.
The degree of order must be limited, for
there seem to be regions that are more or
less chaotic, and there are occasionally
clear breaks between ordered regions, as
if the slabs had been fractured or broken
apart and other parallel arrays inserted
in different directions. These intercalated
slabs may conceivably represent some minor
imperfections in development, or perhaps
they have some special function, as suggested in connection with color by the experiment of figure 8C. It seems likely that cells
concerned with color are arranged in columns (Hubel and Wiesel, '68), and the relationship of these columns to the orientation slabs described in this paper should be
very interesting.
The geometric relationship between ocular-dominance columns and orientation
columns is still not clear, but the fact that
when the electrode crosses from a left-eye
to a right-eye region there is no noticeable
disturbance in the sequence of orientation
columns argues for a certain degree of independence between the two systems. It
would be interesting to know whether the
two sets of slabs are parallel or cut each
other at right angles or have a n y consistent
relationship. We have argued previously
(Hubel and Wiesel, '72, p. 444) that it
would put a great burden on the connections if the two column systems were parallel. A binocular cell with some particular
receptive-field orientation must receive its
input from two sets of monocular cells
having the same receptive-field orientation;
the two sets must, by definition, be located
in separate ocular-dominance columns.
Obviously it is most efficient if the binocular cell and the monocular cells supplying
it are all housed in the same orientation
column, for the alternative - the only one
possible if the two column systems are parallel - is to have connections run from one
orientation column through a n entire array
292
DAVID H. HUBEI, AND TORSTEN N . WIESEL
material most cells are known to have
dendritic and axonal arborizations that extend, apparently in all directions, for distances of up to several millimeters. Perhaps
His tological correlates
the connections made by these processes
It is curious that in contrast to the hori- have a selectivity not hinted at by the anatzontally-running layers, which are obvious omy, for the physiological results predict
at a glance, the boundaries between the strongly that different orientation columns
vertical columnar subdivisions seem not to should not be linked by important excitabe evident by ordinary staining methods. tory connections. Neighboring columns
The ocular-dominance columns are highly might, on the other hand, be linked by indiscrete, especially in layer IV C, yet to hibitory connections subserving movement
identify them histologically has required directional selectivity.br the sharpening of
the use of specialized silver-degeneration response-vs.-orientation tuning curves. At
techniques following laminar geniculate present one can only say that, except for
lesions, a method which depends on the the cortical barrels seen in mice and refact that left-eye and right-eye columns dif- lated species (Woolsey and Van der Loos,
fer because their inputs differ (Hubel and '70), there is no example of a correlation
Wiesel, '72). Orientation columns are dis- between any of the columns yet described
tinguished from each other by differences and the Nissl, Golgi or electron-microscopic
in intracortical connections, and conse- anatomy.
The presence of highly ordered orientaquently no analogous method is possible for
their demonstration. It may be that the tion sequences in area 18 deserves some
vertically running bands of cells are the comment. Area 18 in the monkey receives
slabs cut in transverse section: the mea- a powerful, systematic and orderly projecsurements are consistent with this, for in tion from 17 (Spatz et al., '70), but unlike
the present series the horizontal distance area 18 in the cat it has not been shown to
between shifts was less than double the receive any direct input from the lateral
size of the bands in penetrations in which geniculate body. For example, after small
the two were compared. One would per- discrete lesions made in single dorsal or
haps not expect better agreement, since ventral layers of the geniculate we found
some orientation shifts were probably no obvious Nauta degeneration in area 18,
missed, and the figures for distance between despite a careful search of the parts of 18
shifts were consequently probably over- topographically corresponding to the lesion
estimates. If the vertical bands of cells do sites (Hubel and Wiesel, '72). Other inputs
indeed represent orientation slabs cut in to area 18 in the monkey, for example from
cross section, tangential sections through thalmus outside the geniculate, are at presthe cortex might also be expected to reveal ent conjectural. Thus the only well estabparallel lines of cells, straight or in whorls. lished direct visual input to 18 comes from
In a few observations in the monkey we 17. I t therefore seems likely that a cell in
18 with high orientation specificity derives
have so far seen nothing like this.
In this context the question discussed those properties from cells in 17 having the
above of whether the orientation columns same orientation specificity and receives no
are discrete or merge continuously may be important excitatory inputs from cells with
of some importance; if the variation is in different optimal orientations. By extensome sense continuous one would hardly sion, cells within a given orientation colexpect to find discrete anatomical subdivi- umn must receive most of their inputs from
sions. Perhaps, indeed, the solution to columns with identical orientations in 17.
this problem of discreteness vs. continuity The fact that receptive fields in 18 are sevshould be sought using anatomical rather eral times larger than those in 17 (Hubel
and Wiesel, unpublished) suggests that
than physiological methods.
There is one puzzling apparent discrep- several columns of like orientation specificancy between these physiological results ity in 17 may feed into one column in 18.
and the morphology. The orientationcol- In a n y case, the existence of two similar
umn (or slab) thickness is a t most in the columnar systems in the two visual areas
order of 25-50 P , yet from sections of Golgi implies a specificity of 17-to-18 connections
of intervening columns, stopping only when
they reach the next column subserving the
same orientation.
ORIENTATION COLUMNS I N MONKEY STRIATE CORTEX
far transcending a mere region-to-region
projection.
Biological advantages of ordered
orientation columns
What advantage can such a n ordered
system of orientation columns be to the
animal? We have suggested before that an
economy of connections may result if columns subserving very similar orientations
are close together. To build a simple receptive field from a set of geniculate afferents whose “on” or “off” field centers are
arranged along a line calls for a specific set
of convergent connections. By dropping a
few geniculate inputs and adding a few,
the orientation of the line can be changed
slightly, but the inputs to the old line and
the new will still be largely the same. On
the other hand, two overlapping simple receptive fields with very different orientations would have far fewer afferents in
common. Undoubtedly the wiring is made
simpler and more efficient if cells with similar inputs are close together.
A second possible advantage is related
to the suggestion by Blakemore and Tobin
(‘72) that orientation selectivity may be
sharpened by a cell’s receiving inhibitory
inputs from cells with slightly different
orientations, in a fashion analogous to the
surround inhibition of receptive fields of
retinal ganglion cells and geniculate cells.
Again it would be an advantage, in terms
of efficiency of wiring, if the interconnected cells could be kept close together. Psychophysical observations (Blakemore et al.,
’70) support the idea of mutual inhibition
between neighboring orientation columns,
but it is difficult to think of a direct way
of testing this physiologically. Although
Blakemore’s experiments showing an inhibitory effect from a grid of lines moving
outside the activating part of a cortical
receptive field are suggestive, his results
can also be explained by supposing that
the cells he describes have hypercomplex
properties.
A s a third possibility, an orderly arrangement of columns may have advantages for
development. Perhaps the order reflects a
mechanism for guaranteeing that all orientations be represented once or only a few
times in each part of the visual field, with
no omissions and minimal redundancy. In
this connection, the third paper in this se-
293
ries presents evidence that the entire ordered system is innately determined, and
does not depend for its development on early
experience (Hubel and Wiesel, ’74b).
ACKNOWLEDGMENTS
We wish to thank Sandra Spinks, David
Freeman and Claire Wang for technical assistance. The work was supported by NIH
grants 5R01 EY00605 and 5R01 EY00606,
and a grant from the Esther A. and Joseph
Klingenstein Fund, Inc.
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