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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 ' \ -30- .. . . 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, \ -30, \ -60, 0 ... 0.. -0, 90, z / 60, 0 + / 30, z ' o- 8 \ Q t- .. .. -30, an... 0 - 0.. -60, . ... . . .. .. .. .. .... ... .. ..... .. - 90, / 60, / 30, I 0, \ -30, x -60, - 90, ' 60- ' 304z 90 0. ** 8 L4 I 1 .o 1 2 .o I 3.0 I 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- \ -30- \ -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. LITERATURE CITED Bishop, P. O., W. Kozak, W. R. Levick and G. J . Vakkur 1962 The determination of the projection of the visual field on to the lateral geniculate nucleus in the cat. J. Physiol., 163: 5 0 3 5 3 9 . Blakemore. C., and E. A. Tobin 1972 Lateral inhibition between orientation detectors in the cat’s visual cortex. Exp. Brain Res., 15: 4 3 9 4 4 0 . Blakemore, C.. R. H. S. Carpenter and M. A. Georgeson 1970 Lateral inhibition between orientation detectors in the human visual system. Nature, 228: 37-39. Daniel, P. M., and D. 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