The Specialization of the Owl

Monkey Retina for Night Vision

Luiz Carlos L. Silveira,1* Elizabeth S. Yamada,1

Edna Cristina S. Franco,1 Barbara L. Finlay2
1
Departamento de Fisiologia, Universidade Federal do Pará, 66075-900 Belém, Pará, Brasil

2
Department of Psychology and Neurobiology and Behavior, Uris Hall, Cornell University, Ithaca, NY 14853

Received 28 August 1999; accepted 27 October 1999

Abstract: The anatomy of the owl monkey (Aotus) retina is
reviewed and compared with that of one of its diurnal
relatives, the capuchin monkey (Cebus). A mechanism is
suggested by which the owl monkey has biased its retinal
organization towards a conformation most advantageous
for scotopic vision. © 2000 John Wiley & Sons, Inc. Col Res Appl, 26,
S118 –S122, 2001
Key words: photoreceptors; M and P ganglion cells; fovea;
retina; Aotus; Cebus; primates; night vision
INTRODUCTION
The New World monkeys (Infraorder Platyrrhini, Suborder
Anthropoidea) offer a unique opportunity to perform com-
parative studies about the anthropoid visual system. There
are diurnal and nocturnal species of Platyrrhini that are
closely related in phylogenetic terms. The Subfamily Aoti-
nae, with a single genus Aotus, encompasses as many as
seven different species, and comprises all the living noctur-
nal anthropoid primates.1,2 Together with five genus of
Callitrichinae and two genus of Cebinae, all diurnal, Aotus
belongs to the Family Cebidae.3
We have studied aspects of the retinal organization in
primates that can be related to adaptation to their diurnal or
nocturnal behavior. We have used anatomical methods to
study several neuronal populations of the retina of the owl
monkey (Aotus) and from one of its diurnal relatives, the
capuchin monkey (Cebus).4-10 In the present article, we
* Correspondence to: Dr. Luiz Carlos de Lima Silveira, Departamento
de Fisiologia, Centro de Ciências Biológicas, Universidade Federal do
Pará, 66075-900 Belém, Pará, Brasil (e-mail: luiz@ufpa.br)
Contract grant sponsors: CNPq/NSF; Contract grant number: 910149/
96-8; FINEP/FADESP; Contract grant number: 66.94.0034.00; PRONEX/
FUJB; Contract grant number: 76.97.1028.00
© 2000 John Wiley & Sons, Inc.
reviewed these results and suggest a mechanism by which
the owl monkey has biased its retinal organization towards
a conformation most advantageous for scotopic vision.
CENTRAL SPECIALIZATION
As observed in other diurnal anthropoids, the capuchin
monkey possesses a well-developed fovea.4 The ganglion
cell layer shows a progressive thickening towards the fovea,
reaching several rows of cells in the clivus. The foveola is
devoid of ganglion and bipolar cells. On the other hand, the
majority of the owl monkeys shows only a small depression
temporal to the optic disk, which has the form of a rudi-
mentary fovea.5,11 Within this region, the ganglion cell layer
is thinner and the ganglion cell density is lower than in the
immediate surrounds. In a few owl monkeys, the central
specialization takes the form of an area centralis, and the
ganglion cell density peaks in its center.5,11,12 In either case,
the large vessels and thick nerve fiber bundles avoid this
central region, making it readily identifiable.5,11,13
GANGLION CELL DENSITY DISTRIBUTION
The owl monkey retina has about one-third of the ganglion
cell number found in the capuchin monkey retina.4,5 The
total number of ganglion cells varies from 421,500 –508,700
in the owl monkey and 1,340,000 –1,400,000 in the capu-
chin monkey. These figures were obtained by counting
ganglion cell bodies in whole-mounted retina stained with
cresyl violet. Retrograde labeling from optic-nerve deposits
of horseradish peroxidase provided additional support to the
criteria used to identify and count the ganglion cells.14 In
both species, the highest ganglion-cell density occurs in the
central region and then decreases towards retinal periphery,
but the owl monkey retina has a lower ganglion cell density
than the capuchin monkey retina at all eccentricities [Fig.

S118 COLOR research and application

FIG. 1. Comparison between owl monkey (Aotus) and capuchin monkey (Cebus) retinas. Density and size of retinal neurons
are given as the ratio between the values for the owl monkey and those for the capuchin monkey. Cones and ganglion cells
occur at lower density in the owl monkey than in the capuchin monkey, while rods occur a higher density and ganglion cells
have larger dendritic fields in the owl monkey than in the capuchin monkey. These differences are more conspicuous in the
central region, where the ratio is maximally different from one, while, in the retinal periphery, the ratio tend towards unity. Thus,
evolution towards diurnal and nocturnal life affects maximally the primate central vision. (A)–(B) Total density of (GC) ganglion
cells, density of (MGC) M ganglion cells, and cone density for nasal and temporal retinal quadrants, respectively. (C)–(D)
Dendritic field area of (MDF) M and (PDF) P ganglion cells and rod density for nasal and temporal quadrants, respectively.
Note that a similar ratio for cone density and ganglion cell density implies in similar cone convergence to ganglion cells in both
species, while similar ratio for rod density and ganglion cell dendritic field implies larger rod convergence to ganglion cells in
the owl monkey retina.

1(A)–(B)]. In the central retinal region, ganglion cell den-
sity reaches about 15,000/mm2 in the owl monkey and
49,000/mm2 in the capuchin monkey.
GANGLION CELL CLASSES
The ganglion cells of the capuchin monkey and owl monkey
were also studied by labeling them with biocytin deposited
in the optic nerve.6,8-10 This technique allows for an exten-
sive retrograde filling of retinal ganglion cell axons, somata,
and dendritic trees. Very fine dendritic branches are labeled,
and the results are comparable in many cases to those
obtained with intracellular injections of neurotracers or the
Golgi method.15
The majority of the labeled ganglion cells in the owl
monkey and capuchin monkey retinas are M or P cells.6,8-10
Other less numerous cell classes with morphology corre-
sponding to the wide-field ganglion cells observed in other
anthropoids15,17 were also labeled in both species.9 Small
bistratified cells, which are associated with the blue-yellow
opponent pathway,18,19 were labeled only in the capuchin
monkey retina.9,20
Soma and dendritic field sizes of M and P ganglion cells
of the owl monkey and capuchin monkey retinas were
measured along the horizontal meridian at increasing dis-
tances from the fovea. For all eccentricities, at both tempo-
ral and nasal retina, the M and P ganglion cells from the
capuchin monkey have similar soma and dendritic field size
as those measured in other diurnal anthropoids such as the
macaque monkey.8,9 However, in the owl monkey retina,
both cell classes are larger than their diurnal counterparts at
all eccentricities9,10 [Fig. 1(C)–(D)]. In the owl monkey, the
dendritic field size of M ganglion cells varies from 700 ␮m2
close to the rudimentary fovea to about 225,000 ␮m2 at the
retinal periphery, while that of P ganglion cells varies from
40 ␮m2 to about 40,000 ␮m2. In the capuchin monkey, the
dendritic field size of M ganglion cells varies from 270 ␮m2
close to the fovea to about 140,000 ␮m2 at the retinal

Supplement Volume 26, 2001 S119

periphery, while that of P ganglion cells varies from 14 ␮m2
to about 17,000 ␮m2.
M ganglion cells were also studied in retinal whole
mounts stained by the method of Gros–Schultze.7 This
technique allows for the selective staining of M ganglion
cells, making it possible to estimate their density distribu-
tion.21,22 The owl monkey retina has about 74,000 M gan-
glion cells, half the number of M ganglion cells present in
the capuchin monkey retina, 140,300.7 In both species, the
highest M ganglion cell density occurs in the central region
and then decreases towards retinal periphery, but the owl
monkey retina has a lower M ganglion cell density than the
capuchin monkey retina at all eccentricities [Fig. 1(A)–(B)].
PHOTORECEPTORS
Owl monkey cones and rods have been counted using
tangential retinal sections23 or retinal whole mounts.10,24
These studies agreed extensively for cone and rod density in
most of retinal eccentricities, but Yamada et al.,10 using
retinal whole mounts prepared by the method of Curcio et
al.,25 provided higher values for peak cone density. The owl
monkey has lower cone density and higher rod density than
the capuchin monkey both in the central and peripheral
retinal regions [Fig. 1(A)-(D)].10 In the owl monkey, cone
density reached 16,600 –19,500/mm2 in the central region,
decreasing to about 4,000/mm2 in the nasal and 2,000/mm2
in the temporal periphery. Rod density reached 385,700 –
465,800/mm2 in the central region, decreasing to 150,000/
mm2 and 80,000/mm2 in the nasal and temporal periphery,
respectively. In the capuchin monkey, cone density reached
140,600 –175,800/mm2 in the foveola, decreasing to about
7,300/mm2 and 5,000/mm2 in the nasal and temporal pe-
riphery, respectively. Rods were absent in the fovea, reach
their peak density at midperiphery, 3– 6 mm from the fovea,
120,100 –173,800/mm2, decreasing to 67,800/mm2 and
59,800/mm2 in the nasal and temporal periphery, respec-
tively.
Due to its higher rod density, rod convergence to M and
P ganglion cells is larger in the owl monkey than in the
capuchin monkey.10 In the central retina, at about 1 mm
from the fovea, rod convergence to M cells in the owl
monkey is 1,300 rods/cell in the nasal region and 1,800
rods/cell in the temporal region. For the capuchin monkey,
the rod convergence to M cells at the same eccentricity is 80
rods/cell for both nasal and temporal regions. In the periph-
ery, rod convergence to M cells in the owl monkey reaches
17,700 rods/cell in the nasal region and 17,100 rods/cell in
the temporal region, while for the capuchin monkey these
numbers are 4,700 and 6,500 rods/cell for nasal and tem-
poral regions.
For P cells, the rod convergence in the central retina of
the owl monkey is 130 rods/cell in the nasal region and 110
rods/cell in the temporal region. For the capuchin monkey,
the rod convergence to P cells at the same eccentricity is
much lower: 4 rods/cell in the nasal region and 7 rods/cell
in the temporal region. In the peripheral retina, rod conver-
gence to P cells in the owl monkey is 3,100 rods/cell in the
S120
nasal region and 4,000 rods/cell in the temporal region. For
the capuchin monkey, the rod convergence to P cells at the
same eccentricity is 600 rods/cell in the nasal region and
900 rods/cell in the temporal region.
On the other hand, owl monkey and capuchin monkey
have similar cone convergence to M and P ganglion cells.10
This is a consequence of the larger ganglion cell dendritic
field and lower cone density of the owl monkey retina when
compared with the capuchin monkey retina. These two
parameters change across retinal eccentricity in such a way
that they fairly compensate each other, resulting in a similar
cone convergence to M and P ganglion cells in both species.
In the central retina, at about 1 mm from the fovea, cone
convergence to M cells in the owl monkey is 30 cones/cell
in the nasal region and 40 cones/cell in the temporal region.
For the capuchin monkey, the cone convergence to M cells
at the same eccentricity is 20 cones/cell for both nasal and
temporal regions. In the periphery, cone convergence to M
cells in the owl monkey reaches 500 cones/cell in the nasal
region and 400 cones/cell in the temporal region, while for
the capuchin monkey these numbers are 500 cones/cell for
nasal and temporal regions.
For P cells, the cone convergence in the central retina of
the owl monkey is 2-3 cones/cell for nasal and temporal
regions, while for the capuchin monkey at the same eccen-
tricity it is 1 cone/cell in the nasal and temporal regions. In
the peripheral retina, cone convergence to P cells in the owl
monkey is 80 cones/cell in the nasal region and 100 cones/
cell in the temporal region. For the capuchin monkey, the
cone convergence to P cells at the same eccentricity is 60
cones/cell in the nasal and temporal regions.
Figure 1 summarizes the differences of retinal morphol-
ogy between the nocturnal owl monkey and the diurnal
capuchin monkey. Cones and ganglion cells occur at lower
density in the owl monkey than in the capuchin monkey,
while rods occur a higher density and ganglion cells have
larger dendritic fields in the owl monkey than in the capu-
chin monkey. These differences are more conspicuous in the
central region, while in the retinal periphery the two retinas
are more similar to each other. Thus, evolution towards
diurnal and nocturnal life affects maximally the primate
central vision.
DISCUSSION
In the capuchin monkey, the size of P ganglion cell dendritic
fields, cone density, and bipolar cell morphology and size is
consistent with the presence of a one-to-one midget path-
way for the central vision of this primate,26 as it has been
described for other diurnal anthropoids.27-30 This neural
circuit constitutes the basis for red-green colour opponency
of trichromatic primates, but may have evolved originally
for spatiotemporal achromatic vision.31,32 The owl monkey
P ganglion cells are larger than those of the capuchin
monkey, but the cone convergence to P ganglion cells is
compatible with the presence of a one-to-one pathway also
in the retina of this species. Ogden33 found midget bipolar
cells in the owl monkey retina, but reported that the majority
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of them contacted more than one cone. Additional studies of
the bipolar cell morphology in the central retinal region of
this primate are necessary. The presence of M and P gan-
glion cells in all the primates so far studied, including the
owl monkey and bush baby,34 gives additional support to
the hypothesis that these two cell classes evolved for the
needs of achromatic vision.
In the capuchin monkey, as for the majority of platyr-
rhines, all the males and about one third of females are
dichromats.35-37 There are two cone classes in their retinas,
the SWS- (short-wavelength sensitive) cone and one MWS/
LWS- (medium- to long-wavelength sensitive) cone. About
two-thirds of females are trichromats, possessing the SWS-
cone and two MWS/LWS-cones. This is due to the presence
in these platyrrhines of a single gene locus on the X-chro-
mosome that codes for the MWS/LWS-cone photopig-
ments, associated to gene polymorphism, allowing the
males and homozygotic females to be dichromat and het-
erozygotic females to be trichromats.38 The owl monkey is
an exception to the most common platyrrhine pattern, being
monochromat. The gene on the chromosome 7 that codes
for SWS-cone photopigments is nonfunctional,39 there are
no SWS-cones in the retina,24 and no evidence for SWS-
cone signals from behavioral measurements of visual ca-
pacity.40 Moreover, there is a single gene locus on the
X-chromosome but no gene polymorphism. Consequently,
all the owl monkeys have a single MWS-cone class in their
retinas.
Comparison of the distribution of rods and cones in the
owl monkey and the capuchin monkey reveals functional
morphologies quite suited to their niches. The owl monkey
large eye and increased rod-to-ganglion cell convergence is
suitable for maximizing light catch in the nocturnal niche.
The owl monkey is quite a small monkey, compared to the
capuchin monkey. It is less than a third of the size, only
about 800 g compared to capuchin monkey’s 3,000 g. Yet,
its eye and retinal area is larger (660 mm2 vs. 602 mm2) and
it has managed to dispose of an entire class of cone and
flatten out a fovea, a nocturnal blind spot. It is not clear what
purpose the loss of the SWS-cone might serve intrinsically.
Though nocturnal, the owl monkey remains active a con-
siderable portion of the photopic period. Since the SWS-
cones are a very small population to begin with, and might
serve some useful function in photopic light levels, why
remove them?
We suggest that loss of this cone is the mechanism by
which the owl monkey has gained its useful large eye and
loss of fovea, biasing its eye toward the conformation most
advantageous for the night in which it spends most of its
time. It is well known that the growing eye uses activity to
match its axial length to the power of its optics, a process
called emmetropisation.41 If the image is defocused in the
day, producing a low-contrast image, retinal cells are inac-
tive and the eye grows until a high-contrast image is
achieved. In other words, activity checks the growth of the
eye, and, in diurnal vision, that activity must derive from
cones. Loss of cones could thus produce a component of the
owl monkey’s large eye size.
Supplement Volume 26, 2001
We speculate that activity originating in SWS-cones also
operates earlier to initiate the production of the foveal
specialization. Though mechanisms for general control of
eye growth are unknown, a strong hypothesis with consid-
erable empirical support is that activity acts locally to mod-
ulate retinal and choroidal elasticity.42 Since some aspects
of foveal morphology are present at birth, and dark rearing
has no major effects on foveal morphology in monkeys,43,44
we propose that it is the spontaneous activity and not
experience-related activity of cones that might be involved
in the initial organization of the fovea. Foveal cones are the
first cells produced in the embryonic retina,45 and we pro-
pose that their spontaneous activity in early foetal life serves
to stabilize a retinal area of high cone density that may later,
by elastic forces operating over a nonuniform substrate,
produce the fovea.46
One may speculate whether the primordial anthropoid
was more like the nocturnal owl monkey or the diurnal
capuchin monkey. The available evidences favor the latter
possibility. The seven clades of extant platyrrhines, Aotinae
among them, diverged during the early to middle Miocene,
23–16 MYA.3,47 The cranial remains of very primitive Ao-
tinae from the early Miocene indicate that species such as
Tremacebus harringtoni and Homunculus patagonicus,
were crepuscular or diurnal, respectively. Also, fossil
records reveal the diurnal habit of parapithecids, such as
Apidium phiomense, a group of primitive anthropoids that
existed in the African continent in the late Eocene, 37–31
MYA, and probably preceded the divergence of platyrrhines
and catarrhines.47 All this indicate that the nocturnal way of
life of the genus Aotus appeared long ago in the middle
Miocene, but well after the divergence of platyrrhines and
catarrhines.
ACKNOWLEDGMENTS
Supported by CNPq/NSF #910149/96-8, FINEP/FADESP
#66.94.0034.00, PRONEX/FUJB #76.97.1028.00. LCLS
and ESY have CNPq research fellowships. ECSF has a
CAPES fellowship for graduate students. We thank Dr. José
Augusto P. Muniz, Head of the Centro Nacional de Primatas
for providing the monkeys used in this study. We thank
Cezar Akiyoshi Saito, Francinaldo Lobato Gomes, and
Walter Augusto de Carvalho for research assistance.
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