Development of Orientation and Ocular 
Dominance Columns in Infant Macaques 
Klaus Obermayer 
Howard Hughes Medical Institute 
SMk-Institute 
La Jolla, CA 92037 
Lynne Kiorpes 
Center for Neural Science 
New York University 
New York, NY 10003 
Gary G. Blasdel 
Department of Neurobiology 
Harvard Medical School 
Boston, MA 02115 
Abstract 
Maps of orientation preference and ocular dominance were recorded 
optically from the cortices of 5 infant macaque monkeys, ranging in 
age from 3.5 to 14 weeks. In agreement with previous observations, 
we found that basic features of orientation and ocular dominance 
maps, as well as correlations between them, are present and robust 
by 3.5 weeks of age. We did observe changes in the strength of 
ocular dominance signals, as well as in the spacing of ocular dom- 
inance bands, both of which increased steadily between 3.5 and 14 
weeks of age. The latter finding suggests that the adult spacing 
of ocular dominance bands depends on cortical growth in neonatal 
animals. Since we found no corresponding increase in the spacing 
of orientation preferences, however, there is a possibility that the 
orientation preferences of some cells change as the cort;.cal surface 
expands. Since correlations between the patterns of orientation 
selectivity and ocular dominance are present at an age, when the 
visual system is still immature, it seems more likely that their de- 
velopment may be an innate process and may not require extensive 
visual experience. 
543 
544 Obermayer, Kiorpes, and Blasdel 
I INTRODUCTION 
Over the past years, high-resolution images of the simultaneous representation of 
orientation selectivity and ocular dominance have been obtained in large areas of 
macaque striate cortex using optical techniques [3, 4, 5, 6, 12, 18]. These studies 
confirmed that ocular dominance and orientation preference are organized in large 
parts in slabs. While optical recordings of ocular dominance are in accordance with 
previous findings, it turned out that iso-orientation slabs are much shorter than 
expected, and that the orientation map contains several other important elements 
of organization - singularities, fractures, and saddle-points. 
A comparison between maps of orientation preference and ocular dominance, which 
were derived from the same region of adult monkey striate cortex, showed a pro- 
nounced relationship between both patterns [5, 12, 13, 15, 17]. Fourier analyses, 
for example, reveal that orientation preferences repeat at closer intervals along the 
ocular dominance slabs than they do across them. Singularities were found to align 
with the centers of ocular dominance bands, and the iso-orientation bands, which 
connect them, intersect the borders of ocular dominance bands preferably at angles 
close to 90  . 
Given the fact that these relationships between the maps of orientation and ocular 
dominance are present in all maps recorded from adult macaques, one naturally won- 
ders how this organization matures. If the ocular dominance slabs were to emerge 
initially, for example, the narrower slabs of iso-orientation might later develop in 
between. This might seem likely given the anatomical segregation which is apparent 
for ocular dominance but not for orientation [9]. However, this possibility is contra- 
dicted by physiological studies that show normal, adult-like sequences of orientation 
preference in the early postnatal weeks in macaque when ocular dominance slabs 
are still immature [19]. The latter findings suggest a different developmental hy- 
pothesis; that the organization into regions of different orientation preferences may 
precede or even guide ocular dominance formation. A third possibility, consistent 
with both previous results, is that orientation and ocular dominance maps form 
independently and align in later stages of development. 
In order to provide evidence for one or the other hypothesis, we investigated the 
relationship between ocular dominance and orientation preference in very young 
macaque monkeys. Results are presented in the remainder of this paper. Section 2 
contains an overview about the experimental data, and section 3 relates the data 
to previous modelling efforts. 
2 
ORIENTATION AND OCULAR DOMINANCE 
COLUMNS IN INFANT MACAQUES 
2.1 THE OVERALLSTRUCTURE 
Figure 1 shows the map of orientation preference (Fig. la) and ocular dominance 
(Fig. lb) recorded from area 17 of a 3.5 week old macaqueJ Both maps look similar 
 For all animals orientation and ocular dominance were recorded from a region close to 
the border to area 18 and close to midline. 
Development of Orientation and Ocular Dominance Columns in Infant Macaques 545 
a b 
'"':'1'"'-":':::'"' - -' :::: ::::'-" :.::i;'::::::: ::::': '"':" :':':':':' 
x..%'-.'q-: ..... eeo'.'.o.  '-'-  '.- '.'o' .' '.' '.'  
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;..'-:o:.. . it:: I:: i:.'>  .i.z..:.;'- 
'"':":': .... :':':': ...... .:.i.'"'"' :.:.:-:.it:::. 
Figure 1: Spatial pattern of orientation preference and ocular dominance recorded 
from area 17 of a macaque, 3.15 weeks of age. Figures (a) and (b) show orientation 
preferences and ocular dominance bands within the same 3.1 mm x 4.3 mm large re- 
gion of striate cortex. Brightness values in Fig. (a) indicate orientation preferences, 
where the interval of 180  is represented by the progression in colors frmn black 
to white. Brightness values in Fig. (b) indicate ocular dominance, where bright 
and dark denote ipsi- and contralateral eye-preference. respectively. The data was 
recorded from a region close to the border to area 18 and close to midline. Figure 
(c) shows an enlarged section of this map in the preference (left) and the in contour 
plot (right) representations. Iso-orientation lines on the right indicate intervals of 
11.215 . Letters indicate linear zones (L), saddle points (H), singularities (S), and 
fractures (F). 
to maps which have been recorded from adults. The orientation map exhibits all of 
the local elements which have been described [12, 13]: linear zones, saddle points, 
546 Obermayer, Kiorpes, and Blasdel 
a 
.1= 6121un 
to area 17/18 b 1.2 
boiler 1.0 = Opm 
 o  0.2 
::: ::: :::: X. = 7241m 0.0 - . , . 
0 I 2 3 4 5 
spatial frequency [1/mm] 
c e 0.5 
.o [ 
o.o 
-0.5 
0 200 400 600 800 
distance [gm] 
Figure 2: Fourieranalysis of the ori- 
entation map shown in Figure la. 
(a) Complex 2D-Fouriertransform. 
Each pixel corresponds to one Fouri- 
ermode and its blackness indicates 
the corresponding energy. A dis- 
tance of one pixel corresponds to 
0.23/mm. (b) Power as a function 
of radial spatial frequency. (c) Au- 
tocorrelations $ii as a function of 
distance. The indices i,j E {3,4} 
denote the two cartesian coordinates 
of the orientation preference vector. 
For details on the calculation see 
[13, 15]. 
singularities, and fractures (Fig. lc). The ocular dominance map shows its typical 
pattern of alternating bands. 
Figure 23 shows the result of a complex 2D Fourier transform of the orientation 
map shown in Figure la. Like for maps recorded from adult monkeys [13] the 
spectrum is characterized by a slightly elliptical band of modes which is centered 
at the origin. The major axis approximately aligns with the axis parallel to the 
border to area 18 as well as with the ocular dominance bands. Therefore, like in 
the adults, the orientation map is stretched perpendicular to the ocular dominance 
bands, apparently to adjust to the wider spacing. 
When one neglects the slight anisotropy of the Fourier spectra one can estimate a 
power spectrum by averaging the squared Fourier amplitudes for similar frequen- 
cies. The result is a pronounced peak whose location is given by the characteristic 
frequency of the orientation map (Fig. 2b). As a consequence, autocorrelation func- 
tions have a Mexican-hat shape (Fig. 2c), much like it has been reported for adults 
[13, 15]. 
In summary, the basic features of the patterns of orientation and ocular dominance 
are established as early as 3.5 weeks of age. Data which were recorded from four 
Development of Orientation and Ocular Dominance Columns in Infant Macaques 547 
Table 1: Characteristic wavelengths ("OD) and signal strengths (O'OD) for the ocular 
dominance pattern, as well as characteristic wavelengths (AoP), density of +180 - 
singularities (p+), density of - 180-singularities (p_), total density of singularities 
(p), and percentage of area covered by linear zones (ali,) for the orientation pattern 
as a function of age. 
age (rOD AOD AOp p+ p- p aim 
(weeks) (pm) (pm)(mm -2) (mm -2) (mm -2) (%area) 
3.5 0.92 686 660 3.9 3.9 7.8 47 
5.5 0.96 730 714 3.7 3.7 7.4 49 
7.5 0.66 870 615 4.5 4.5 9.0 45 
14 1.23 917 700 3.9 3.8 7.7 36 
adult 1.36 950 768 3.9 3.8 7.7 43 
other infants ranging from 5.5 to 14 weeks (not shown) confirm the above findings. 
2.2 
CHARACTERISTIC WAVELENGTHS AND SIGNAL 
STRENGTH 
A more detailled analysis of the recorded patterns, however, reveals changes of 
certain features with age. Table 1 shows the changes in the typical wavelength of 
the orientation and ocular dominance patterns as well as the (normalized) ocular 
dominance signal strength with age. The strength of the ocular dominance signal 
increases by a factor of 1.5 between 3.5 weeks and adulthood, a fact, which could 
be explained by the still ongoing segregation of fibers within layer IVc. 
The spacing of the ocular dominance columns increases by approximately 30% be- 
tween 3.5 weeks and adulthood. This change in spacing would be consistent with 
the growth of cortical surface area during this period [16] if one assumes that cor- 
tex grows anisotropically in the direction perpendicular to the ocular dominance 
bands. Interestingly, the characteristic wavelengths of the orientation patterns do 
not exhibit such an increase. The wavelengths for the patterns recorded from the 
different infants are close to the "adult" values. More evidence for a stable orienta- 
tion pattern is provided by the fact, that the density ofsingularities is approximately 
constant with age 2 and that the percentage of cortical area covered by linear zones 
does neither increase nor decrease. Hence we are left with the puzzle that at least 
the pattern of orientation does not follow cortical growth. 
2.3 
CORRELATIONS BETWEEN THE ORIENTATION AND 
OCULAR DOMINANCE MAPS 
Figure 3 shows a contour plot representation of the pattern of orientation preference 
in overlay with the borders of the ocular dominance bands for the 3.5 week old 
animal. Iso-orientation contours (thin lines) indicate intervals of 15 . Thick lines 
indicate the border of the ocular dominance bands. From visual inspection it is 
2Note that both types of singularities appear in equal numbers. 
548 Obermayer, Kiorpes, and Blasdel 
Figure 3: Contour plot representa- 
tion of the orientation map shown in 
Figure la in overlay with the borders 
of the ocular dominance bands taken 
from Figure lb. Iso-orientation lines 
(thin lines) indicate intervals of 15  . 
The borders of the ocular dominance 
bands are indicated by thick lines. 
already apparent that singularities have a strong tendency to align with the center 
of the ocular dominance bands (arrow 1) and that in the linear zones (arrow 2), 
where iso-orientation bands exist, these bands intersect ocular dominance bands at 
angles close to 90  most of the time. 
Table 2 shows a quantitative analysis of the local intersection angle. Percentage 
of area covered by linear zones (cf. [12] for details of the calculation) is given for 
regions, where orientation bands intersect ocular dominance bands within 18  of 
perpendicular, and regions where they intersect within 18  of parallel. For all of 
the animals investigated the percentages are two to four times higher for regions, 
where orientation bands intersect ocular dominance bands at angles close to 90 , 
much like it has been observed in adults [12]. In particular there is no consistent 
trend with age: the correlations between the orientation and ocular dominance 
maps are established as early as 3.5 weeks of age. 
age p e rp ap a r 
alin lin 
(weeks) (%area)(% area) 
3.5 15.9 4.1 
5.5 12.2 6.8 
7.5 13.3 6.2 
14 12.4 3.7 
adult 18.0 2.7 
Table 2: Percentage of area covered by 
linear zones as a function of age for re- 
gions, where orientation bands inter- 
sect ocular dominance bands within 
18  of perpendicular (%Pin, P), and re- 
gions where they intersect within 18  
of parallel ta p"" (cf. [12] for details of 
\ lin ] 
the calculation). 
Development of Orientation and Ocular Dominance Columns in Infant Macaques 549 
3 CONCLUSIONS AND RELATION TO MODELLING 
In summary, our results provide evidence that the pattern of orientation is estab- 
lished at a time when the pattern of ocular dominance is still developing. However, 
they provide also evidence for the fact that the pattern of orientation is not linked 
to cortical growth. This latter finding still needs to be firmly established in studies 
where the development of orientation is followed in one and the same animal. But if 
it is taken seriously the consequence would be that orientation preferences may shift 
and that pairs of singularities are formed. The early presence of strong correlations 
between both maps indicate that the development of orientation and ocular dom- 
inance are not independen processes. Both paerns have to adjust to each oher 
while cortex is growing. It, therefore, seems as if the third hypothesis is true (see 
Introduction) which states that both patterns develop independently and adjust to 
each other in the late stages of development. As has been shown in [13, 15] and is 
suggested in [7, 14] these processes are certainly in the realm of models based on 
Hebbian learning. 
Many features of the orientation and ocular dominance maps are present at an age 
when the visual system of the monkey is still immature [8, 11]. In particular, they 
are present at a time when spatial vision is strongly impared. Consequently, it 
seems unlikely that the development of these features as well as of the correlations 
between both patterns requires high acuity form vision, and models which try to 
predict the structure of these maps from the structure of visual images [1, 2, 10] 
have to take this fact into account. The early development of orientation prefer- 
ence and its correlations with ocular dominance make it also seem more likely that 
their development may me an innate process and may not require extensive visual 
experience. Further experiments, however, are needed to settle these questions. 
Acknowledgement s 
This work was funded in part by the Klingenstein Foundation, the McKnight Foun- 
dation, the New England Primate Research Center (P51RRO168-31), the Seaver 
Institute, and the Howard Hughes Medical Institute. We thank Terry Sejnowski, 
Peter Dayan, and Rich Zemel for useful comments on the manuscript. Linda. As- 
comb, Jaqueline Mack, and Gina Quinn provided excellent technical assistance. 
References 
[1] 
[2] 
[3] 
H. G. Barrow and A. J. Bray. Activity induced color blob formation. In 
I. Alexander and J. Taylor, editors, Artificial Neural Networks H, pages 5-9. 
Elsevier Publishers, 1992. 
H. G. Barrow and A. J. Bray. A model of the adaptive development of complex 
cortical cells. In I. Alexander and J. Taylor, editors, Artificial Neural Networks 
//, pages 1-4. Elsevier Publishers, 1992. 
E. Barfield and A. Grinvald. Relationships between orientation-preference pin- 
wheels, cytochrome oxidase blobs, and ocular-dominance columns in primate 
striate cortex. Proc. Natl. Acad. $ci. USA, 89:11905-11909, 1992. 
550 Obermayer, Kiorpes, and Blasdel 
[4] G. G. Biasdel. Differential imaging of ocular dominance and orientation selec- 
tivity in monkey striate cortex. J. Neurosci., 12:3117-3138, 1992. 
[5] G. G. Blasdel. Orientation selectivity, preference, and continuity in monkey 
striate cortex. J. Neurosc,., 12:3139-3161, 1992. 
[6] G. G. Blasdel and G. Salama. Voltage sensitive dyes reveal a modular organi- 
zation in monkey striate cortex. Nature, 321:579-585, 1986. 
[7] R. Durbin and G. Mitchison. A dimension reduction framework for under- 
standing cortical maps. Nature, 343:644-647, 1990. 
[8] L. Kiorpes and T. Movshon. Behavioural analysis of visual development. In 
J. R. Coleman, editor, Development of Sensory Systems n Mammals, pages 
125-154. John Wiley, 1990. 
[9] S. LeVay, D. H. Hubel, and T. N. Wiesel. The development of ocular dominance 
columns in normal and visually deprived monkeys. J. Comp. Neurol., 191:1-51, 
1980. 
[10] Y. Liu and H. Shouval. Principal component analysis of natural images - an 
analytic solution. Preprint. 
[11] T. Movshon and L. Kiorpes. Biological limits on visual development in pri- 
mates. In K. Simon, editor, Handbook of bfant Vision. Oxford University 
Press, 199.3. in press. 
[12] K. Obermayer and G. G. Biasdel. Geometry of orientation and ocular domi- 
nance columns in monkey striate cortex. J. Neurosci., 13:4114-4129, 1993. 
[13] K. Obermayer, G. G. Blasdel, and K. Schulten. A statistical mechanical analy- 
sis of self-organization and pattern formation during the development of visual 
maps. Phys. Rev. A15, 45:7568-7589, 1992. 
[14] K. Obermayer, H. Ritter, and K. Schulten. A principle for the formation of 
the spatial structure of cortical feature maps. Proc. Natl. Acad. Sci. USA, 
87:8345-8349, 1990. 
[15] K. Obermayer, K. Schulten, and G. G. Blasdel. A comparison of a neural 
network model for the formation of brain maps with experimental data. In 
D. S. Touretzky and R. Lippman, editors, Advances in Neural Information 
Processing Systems 4, pages 83-90. Morgan Kaufmann Publishers, 1992. 
[16] D. Purves and A. LaMantia. Development of blobs in the visual cortex of 
macaques. J. Comp. Neurol., 332:1-7, 1993. 
[17] N. Swindale. A model for the coordinated development of columnar systems 
in primate striate cortex. Biol. Cybern., 66:217-230, 1992. 
[18] D. Y. Tso, R. D. Frostig, E. E. Lieke, and A. Grinvald. Functional organization 
of primate visual cortex revealed by high resolution optical imaging. Science, 
249:417-420, 1990. 
[19] T. N. Wiesel and D. H. Hubel. Ordered arrangement of orientation columns 
in monkeys lacking visual experience. J. Comp. Neurol., 158:307-318, 1974. 
