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Light-dependent retinal innervation of the rat superior colliculus.

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THE ANATOMICAL RECORD 290:341–348 (2007)
Light-Dependent Retinal Innervation of
the Rat Superior Colliculus
Behavioral Neuroscience Program, University of St. Thomas, St. Paul, Minnesota
Department of Comparative Biosciences, University of Wisconsin, Madison, Wisconsin
Department of Psychiatry, University of Wisconsin, Madison, Wisconsin
Mammalian retinal projections are divided into two anatomically and
functionally distinct systems: the primary visual system, which mediates
conscious visual processing, and the subcortical visual system, which
mediates nonconscious responses to light. Light deprivation during a critical period in development alters the anatomy, physiology, and function of
the primary visual system in many mammalian species. However, little is
known about the influence of dark-rearing on the development of the subcortical visual system. To evaluate whether the early lighting environment alters the anatomy of the subcortical visual system, we examined
the retinas and retinofugal projections of rats reared in a 12:12 light/dark
cycle or in constant dark from birth to 4 months of age. We found that
dark-rearing was associated with a reduction in the distribution of retinal
fibers in the stratum opticum of the contralateral superior colliculus. In
contrast to the plasticity of the retinocollicular projection, retinal input to
sleep, circadian, and pupillary control centers in the hypothalamus, pretectum, and lateral geniculate complex was unaffected by dark-rearing. A
decrease in retinal innervation of the stratum opticum and intermediate
layers of the superior colliculus may account for some of the deficits in multisensory integration that have been observed in dark-reared animals of several species. Anat Rec, 290:341–348, 2007. Ó 2007 Wiley-Liss, Inc.
Key words: superior colliculus; dark-rearing; retinofugal projections; subcortical visual system; plasticity
Mammalian retinofugal projections are divided into
two anatomically and functionally distinct systems. The
primary visual system, consisting of the retinorecipient
dorsal lateral geniculate nucleus (dLGN) and the visual
cortex, mediates conscious visual processing; the subcortical visual system, a collection of retinorecipient
nuclei throughout the hypothalamus and midbrain,
mediates non-conscious responses to light, including
entrainment of the circadian rhythm, acute changes in
behavioral state, pupil dilation and constriction, and reflexive movements of the eyes, neck and head (Schneider, 1969; Harrington, 1997; Morin and Blanchard,
Dark-rearing during a critical period in development
has a deleterious effect on the development of the primary visual system in many mammalian species. Beginning with Hubel and Wiesel’s seminal studies on darkreared and monocularly deprived kittens (Hubel and
Wiesel, 1963; Wiesel and Hubel, 1965), substantial
research confirms that a functionally significant portion
of the development of the primary visual system occurs
postnatally and is light- and activity-dependent. Specifically, dark-rearing impairs the development of the
dLGN by reducing the proportion of relay Y-cells (Kratz
et al., 1979; Mower et al., 1981) and by increasing the
convergence of on- and off-center receptive field maps
(Akerman et al., 2002). In the visual cortex, dark-rear-
*Correspondence to: J. Roxanne Prichard, University of St.
Thomas, Mail JRC LL56, 2115 Summit Avenue, St. Paul, MN
55105. Fax: 651-962-5051. E-mail:
Received 27 July 2005; Accepted 4 January 2007
DOI 10.1002/ar.20424
Published online 23 February 2007 in Wiley InterScience (www.
ing impairs development by slowing the maturation of
glia and pruning of neurons (reviewed in Sherman and
Spear, 1982), disrupting columnar and orientation-specific organization (Chapman et al., 1999), impairing tissue vascularization (Argandona and Lafuente, 1996,
2000), and altering gamma aminobutyric acid (GABA)ergic (Benevento et al., 1995) and glutamatergic synaptic transmission (Czepita et al., 1994). Collectively, these
dark-rearing-induced anatomical and physiological changes
in the primary visual system significantly impair visual
processing (Sherman, 1973; Caspy and Babkoff, 1983;
Fagiolini et al., 1994).
By comparison with the dLGN and visual cortex, the
effects of dark-rearing on the subcortical visual system
have received less attention. The neonatal lighting environment has been shown to influence some physiological
properties of neurons in the superior colliculus (SC), a
laminated structure that receives topographically organized inputs encoding visual, auditory, and somatosensory
stimuli, and that orchestrates multiple immediate motor
responses to these stimuli (Huerta and Harting, 1984;
Stein et al., 1993; McHaffie et al., 2002).
For example, dark-rearing is associated with a nonreversible loss in directionality and binocular convergence
in neurons of the cat superior colliculus (WickelgrenGordon, 1972; Hoffman and Sherman, 1975; Flandrin
and Jeannerod, 1977). In rodents, dark-rearing has been
shown to slow the developmentally regulated increase in
apoptotic neurons in the mouse SC (Sasaki et al., 1999)
and reduce receptive field refinement in the rat SC
(Binns and Salt, 1997). However, very little is known
about the influence of early light exposure on the development of retinofugal projections per se to the SC and
other nuclei of the subcortical visual system.
Research from our laboratory has shown that sleep
responses to light and dark are influenced by dark-rearing; specifically, dark-rearing enhances dark pulse-induced REM sleep triggering (Prichard et al., 2004), a
phenomenon mediated by the pretectal nuclei in albino
rats (Miller et al., 1999). Similarly, dark-reared rats
have a delayed acquisition of circadian rhythm, as compared to light-dark (LD)-reared rats (Cambras and DiezNoguera, 1991). Given that the anatomy and physiology
of the primary visual system is disrupted by dark-rearing, and that sleep and circadian responses to light
mediated by the subcortical visual system are compromised by dark-rearing, we hypothesized that darkrearing might influence the development of retinofugal
projections to the subcortical visual system. To test this
hypothesis, we used the highly sensitive anterograde
tracer cholera toxin b (CTb) to label retinal projections
in dark- and LD-reared rats. The results from this
experiment provide the first systematic investigation of
the effects of dark-rearing on retinal input to the rat
subcortical visual system.
Albino rats (Charles River F344) were reared in either
constant dark (DD; 0 lux) or in a control 12:12 LD environment (lights-on at 06:00, 65 lux; lights-off at 18:00, 0
lux) from before birth until adulthood (4 months). One
week prior to giving birth, pregnant dams were individually housed in clear acrylic cages (26 cm width 3 40
cm length 3 60 cm height) in the two lighting condi-
tions. Dark-reared rats were totally deprived of light;
the routine care of the DD rats was done by personnel
wearing infrared goggles (D-2MV; R and R International
Trade, Fountain Valley, CA). At postnatal day (P) 21,
dams were removed from the experiment and pups were
housed in same-sex groups of three and had access to
food and water ad libitum throughout the experiment.
Research protocols were approved by the University of
Wisconsin School of Medicine Animal Care and Use
Committee and conform to National Institutes of Health
Although albino rats are known to have several anatomical anomalies in the visual system projections, such
as an enhanced contralateral retinal projection to the
dorsal lateral geniculate nucleus, as compared with pigmented rats (reviewed in Sefton and Dreher, 1995), they
are a valuable model for examining the effects of early
lighting environment on the subcortical visual system.
First, albino rats have an exaggerated and observable
sleep-wake response to acute light-dark shifts, as compared to pigmented rats (Benca et al., 1991, 1998; Obermeyer and Benca, 1999), and sleep and circadian locomotor activity is disrupted in albino rats by dark- and
light-rearing (Canal-Corretger, 2001; Prichard et al.,
2004). Second, the difference in retinofugal projections
between pigmented and albino rats is relatively minor;
of the 13 nuclei in the subcortical visual system, only 4
(the ventral lateral hypothalamus, the commissural pretectal area, the posterior limitans, and the intergeniculate leaflet) show a quantifiable enhancement of contralateral retinal input in albino versus pigmented rats
(Fleming et al., 2006).
In order to visualize retinofugal projections, nine DD
and eight LD rats were injected intraocularly with the
anterograde tracer CTb (0.4 ml; List Biologicals) at 4
months of age in their home lighting environment (DD
or LD), as described previously (Prichard et al., 2002).
CTb, which does not travel transsynaptically (Coolen
et al., 1999), was chosen for its superior uptake, sensitivity, rapid transport, and frequent use in analysis of
the retinohypothalamic tract (Angelucci et al., 1996). After a 5-day survival in their home lighting environment
(LD or DD), rats were euthanized by overdose with sodium pentobarbital (1.0 mg/kg, i.p.), received heparin
intracardially (0.07 mg/kg), and were perfused transcardially with 500 ml of cold 4% paraformaldehyde (pH
7.4). DD rats were euthanized in the dark, and their
eyes were bandaged to prevent exposure to light during
the perfusion. Brains and eyes were dissected and stored
overnight at 48C, then cryoprotected (20% sucrose and
5% glycerin in 0.1 M phosphate buffer) for 24 hr at 48C.
Eyes were embedded in paraffin, sectioned sagitally at
10 mm, and stained with hematoxylin and eosin. Brains
were sectioned coronally at 50 mm. Sequential sections
through the diencephalon and mesencephalon were reacted with antisera to CTb (goat; 1:20,000; List Biologicals; visualized with 0.04% 3,30 -diaminobenzidine). Tissues from LD and DD animals were reacted on the same
day, and negative controls were run concurrently. For
illustration purposes, image quality was optimized by
making selected adjustments in gamma, brightness, and
contrast using Photoshop version 6.0 software.
To evaluate the patency of retinal projections to subcortical visual nuclei, 12–15 representative coronal sections from the level of the optic chiasm to the caudal
pole of the SC were examined in animals in each rearing
condition. Rats were removed from the study (three LD,
three DD) if sections through the SC showed patchy
label in the superficial layer, which would reflect injury
to the retinal ganglion cell layer associated with intraocular injection (Redgrave et al., 1993). Under bright- and
dark-field microscopy, the distribution and density of
CTb label in each of the subcortical visual nuclei was
compared to published reports (Prichard et al., 2002). If
a difference in CTb density or distribution between the
two rearing groups was detected in any retinorecipient
region, a quantitative and qualitative analysis of retinal
terminal density and distribution was performed. Quantitative analysis of pixel intensity was used when the
distribution of retinal terminals was dense and even,
such as in the superficial layers of the superior colliculus; qualitative analysis of the relative staining intensity
was used when the distribution of retinal terminals was
patchy and irregular, such as in the stratum opticum
and intermediate layers of the superior colliculus.
In areas of dense, evenly distributed label in the superior colliculus, digital photographs (16 bit; 65,536 gray
levels) of brain sections were taken using a SPOT camera (Diagnostic Instruments), and quantitative image
analysis was performed with ImagePro Plus software.
All images were obtained under identical bright-field
illumination. Matched sections through the rostral, middle, and caudal regions of the nucleus were photographed. A circular sample area was defined (27,134
mm2) and three optical density measurements (medial,
middle, and lateral) were obtained from the superficial
layers in each section. Optical density, the relative darkness of each pixel, was determined by plotting the mean
intensity level of pixels within the defined area on a
standard optical density curve calibrated to incident
light and dark. To control for background labeling, optical density was measured in a region devoid of stain
(periaqueductal gray) in each section and this value was
subtracted from each measurement of density in that
section. Data were analyzed using a 2 3 3 repeatedmeasures ANOVA (SigmaStat, version 2.0; Jaendel, San
Raphael, CA) with rearing condition (DD or LD) and section level (medial, middle, and lateral) as the variables,
and a ¼ 0.05.
In areas of patchy distribution of retinal staining, two
observers blinded to the identity of the animals examined six matched sections throughout the rostral, middle, and caudal region of the superior colliculus under
bright-field microscopy and ranked the animals according to overall staining density and distribution, from
least to greatest. Rankings from the two observers
showed high interrater reliability (r > 0.90). The mean
ranking of staining intensity was evaluated for statistical significance by a Mann-Whitney U-test, with a ¼
To help delineate nuclear boundaries and laminae,
CTb tracing of retinofugal fibers was used in conjunction
with immunocytochemistry for the calcium binding protein parvalbumin in two animals from each lighting condition (Paxinos et al., 1999). Free-floating 50 mm sections
were incubated overnight at room temperature with primary antibody as previously described (1:60,000; Sigma)
(Prichard et al., 2002).
Histological examination of the retinal ganglion cell
layer was performed on a subset of rats from each of the
rearing conditions (four LD, four DD). Sections through
the eyes were examined for evidence of retinopathy
(thinning of the retinal ganglion cell layer, loss of rods
and cones). Cells in the retinal ganglion cell layer containing well-stained nuclei were counted in LD and DD
rats by two observers blinded to the identity of the rats.
Sample fields measuring 1 mm in diameter were distributed throughout the retina (two central, six peripheral).
Mean cell counts from the two central and the six peripheral fields were compared across rearing groups by
one-way analysis of variance (ANOVA), with a ¼ 0.05.
This sampling technique produced reliable and repeatable counts of retinal ganglion cells, with high interrater
reliability (r > 0.90).
Among the retinofugal targets of subcortical visual
system, dark-rearing had the greatest impact on the
superior colliculus (SC). In the contralateral SC, DD
rats had a reduced retinal input to the stratum opticum
layer in the SC. Additionally, retinofugal fibers in DD
rats did not appear to extend into the intermediate
layers of the contralateral superior colliculus (Fig. 1).
This reduction in retinal input was present throughout
the rostrocaudal and mediolateral extent of the contralateral colliculus. Two observers blinded to the rearing
condition ranked the staining intensity in the stratum
opticum and intermediate gray layer of the SC for each
DD rat (n ¼ 6) as lower than the staining intensity for
each LD rat (n ¼ 5), with the sum of the ranks equal to
21 (S 1–6) for the DD rats and 35 (S 7–11) for the LD
rats (U ¼ 0; P < 0.01). A quantitative analysis of CTb
staining intensity in the superficial layers of the contralateral SC showed no significant difference between LD
and DD rats in retinal input to lateral, middle, or
medial sections of the stratum griseum superficiale layer
(F1,8 ¼ 0.359; P ¼ 0.567; Table 1).
There were no obvious differences in retinal input to
the ipsilateral superior colliculus between the two rearing conditions. Both LD and DD rats had a sparse,
patchy projection to the ipsilateral superior colliculus,
with more stained fibers present in the intermediate
than in the superficial layers, and more patches in the
rostral than the caudal part of the nucleus.
Both ipsilateral and contralateral retinal projections
to the dLGN and all other regions of the subcortical visual system in DD rats appeared normal by comparison
with LD rats and previously published reports (Fig. 2)
(Prichard et al., 2002). No differences in CTb staining
intensity were observed between the two rearing conditions in the hypothalamus, including the suprachiasmatic nucleus (SCN), the subparaventricular zone, and
the ventral lateral preoptic area. Likewise, no differences in retinofugal projections to the ventral lateral geniculate nucleus (vLGN), the intergeniculate leaflet (IGL),
or the pretectum were observed. Pretectal nuclei examined included the olivary pretectal nucleus (OPN), anterior pretectal nucleus, medial pretectal nucleus, nucleus
of the optic tract, the commissural pretectal area, and
the posterior limitans (PLi).
Histological examination of the retinae revealed no
retinopathy in DD rats by comparison with LD rats.
There was no indication of retinal thinning or loss of
rods and cones and counts of retinal ganglion cells in
Fig. 1. Cytoarchitecture and retinal innervation of the superior colliculus (SC) in light-dark-reared rats (A, C, and E) and dark-reared rats
(B, D, and F). A and B: As seen with parvalbumin immunoreactivity,
there is no compression of the superficial gray layer (SGS), the stratum opticum (SO), or the intermediate layer following dark-rearing. C–
F: Cholera toxin b immunoreactive retinal fibers in the contralateral
SC. Note the reduction in labeled fibers in the SO of dark-reared rats
by comparison with light-dark-reared rats (C and D; magnified in E
and F). Scale bars ¼ 250 mm (A and B); 100 mm (C and D); 30 mm (E
and F).
TABLE 1. Mean optical density measurements of
CTb-labeled retinal fibers in the contralateral
stratum griseum superficiale layer of the superior
colliculus. No significant differences in retinal input
to the lateral, middle or medial sections of this layer
were found between light-dark-reared (LD, n 5 5)
and dark-reared (DD, n 5 4) rats.
St. Dev.
All Samples
All samples
representative sections from each retina showed no significant differences between rearing groups in the central or peripheral retina (P > 0.05).
The principal finding of this study is that dark-rearing
is associated with a reduction in retinal input to the contralateral stratum opticum of the SC. In contrast, darkrearing does not appear to influence retinal ganglion cell
density or the distribution of retinofugal projections to
the dLGN or to other nuclei of the subcortical visual system. The rat superior colliculus, which orchestrates multiple immediate motor responses to sensory stimuli,
receives dense retinal input in the stratum griseum
superficiale layer, as well as direct input from retinal
terminals in the stratum opticum (Beckstead and Frankfurter, 1983; Boka et al., 2006), and multisensory inputs
from auditory, somatosensory, and cortical visual sources
in the intermediate and deep layers (Schiller and
Stryker, 1972; Stein and Clamann, 1981; Sahibzada
et al., 1986; Dean et al., 1988; Behan and Kime, 1996).
In particular, neurons in the stratum opticum and the
intermediate layers of the rat SC play an important role
in communication between the sensory superficial layers
and the deep premotor layers by gating synchronous
depolarizations and activating intralaminar pathways
(Saito and Isa, 1999, 2005). In awake behaving rats,
chemical stimulation of the SC results in immediate defensive head movements (Redgrave et al., 1981), and
electrical stimulation of the lateral intermediate layers
of the SC induces horizontal head movements (King
et al., 1991). Patterned firing in neurons of the intermediate layers of the SC likely modulates the transfer of
retinal information during such orienting movements
(Lee et al., 1997; Pettit et al., 1999; Helms et al., 2005;
Lee and Hall, 2006).
The stratum opticum and intermediate layers of the
rodent SC are particularly prone to postnatal reorganization following sensory deprivation. For example, congenitally deaf mice show an increase in retinal axons in
the stratum opticum and in the intermediate layers of
the SC, areas that are usually heavily innervated by
neurons in the inferior colliculus (Hunt et al., 2005).
Furthermore, hamsters with neonatal lesions of the superficial layers of the SC ipsilateral to a monocularly
enucleated eye show significantly increased retinal
innervation of the intermediate layers of the SC, as well
as to other nuclei of the subcortical visual system
(Carman and Schneider, 1992). The reduction in retinal
input that we observed in the stratum opticum of the
SC following dark-rearing could be due to a lack of patterned retinal ganglion cell activity resulting in pruning
of retinal ganglion cell axons, or to a developmental failure to establish synaptic connections followed by a compensatory increase in axonal input from other sensory
modalities (e.g., afferent auditory fibers). Whether one
or both of these situations occur will require further
The capacity of SC neurons to integrate visual, auditory, and somatosensory inputs develops postnatally
(King et al., 1988; Wallace and Stein, 1997), and light
deprivation during development has a negative impact
on this multisensory integration. For example, darkrearing inhibits acoustic spatial map formation in the
SC of ferrets and guinea pigs (Withington, 1992; King
and Carlile, 1993). Similarly, early blind humans show
deficits in sound elevation localization, a task partially
mediated by the SC (Zwiers et al., 2001). Wallace et al.
(2004) reported that dark-rearing disrupts the ability of
multisensory neurons in the intermediate and deep
layers of the SC to integrate bimodal cues in the cat,
although these neurons were still able to respond
robustly to the cross-modal inputs when presented individually. A reduction in retinal input to the stratum
opticum and intermediate layers of the SC during development may underlie such failures in multisensory integration.
In contrast to the reduction in retinal input to the
stratum opticum of the SC following light deprivation,
retinofugal projections to the dLGN and to other subcortical visual nuclei appeared to be unaffected by darkrearing. The robustness of retinal projections to the
hypothalamic and pretectal nuclei of the subcortical visual system is not too surprising, as these projections are
preferentially preserved in the naturally dark-reared
rodent, Spalax ehrenbergi. In this blind mole rat, retinal
input to the SCN and the pretectum is well-developed
by comparison with the dLGN and the SC and is comparable in size to that of land-dwelling rodents (Bronchti
et al., 1991; Cooper et al., 1993). Thus, projections to
these retinorecipient regions seem to be highly conserved, despite natural or induced dark-rearing.
It is possible that the normal variability in CTb staining could have obscured any minor dark-rearing-induced
changes in the intensity of retinal innervation; however,
we observed no changes in the distribution of retinal
input to these nuclei. Furthermore, the quantitative
analysis of optical density showed no significant differences in the superficial gray layer of the SC, the largest
target of retinofugal fibers. Dark-rearing may have
altered bouton size or the number of boutons associated
with each axon, resulting in changes in synaptic efficacy.
Even small changes, beyond our ability to measure with
light microscopic techniques, could potentially have
physiological consequences.
The critical period during which retinal innervation of
the SC can be disrupted by dark-rearing is not yet
known. Retinal ganglion cells are generated between
E13 and E19, and the earliest axons reach the SC by
E16 (Lund and Bunt, 1976; Dallimore et al., 2002).
Fig. 2. Cholera toxin b immunoreactive retinal
fibers in retinofugal targets of the primary and subcortical visual system in light-dark-reared (A, C, and
E) and dark-reared (B, D, and F) rats. The distribution of retinal fibers in the suprachiasmatic nucleus
(SCN), the dorsal lateral geniculate nucleus (dLGN),
intergeniculate leaflet (IGL), ventral lateral geniculate
nucleus (vLGN), olivary pretectal nucleus (OPN),
posterior limitans (PLi), and commissural pretectal
area (CPA) was similar in rats reared in both lighting
conditions. Scale bars ¼ 200 mm (A and B); 400 mm
(C and D); 300 mm (E and F).
Because we observed no evidence of retinopathy or loss
of retinal ganglion cells in the DD rats, we can assume
that the reduction in the retinocollicular projection was
not the direct result of major pathology in the retina
itself. However, dark-rearing has been shown to induce
more subtle changes in retinal anatomy and physiology
(Guenther et al., 2004; Zhang et al., 2005), which might
in turn influence the activity-dependent development of
retinofugal projections, and which might underlie some
of the altered sleep/wakefulness responses to light that
are observed in dark-reared rats (Prichard et al., 2004).
Further studies will be required to determine whether
the reduction of input to the stratum opticum and intermediate gray layers of the SC in DD rats is a result of
impaired axonal arborization, or aberrant remodeling of
an initially diffuse projection, and whether this reduction can be reversed in adulthood by a period of normal
light exposure.
Supported by National Institutes of Health
MH52226 (to R.M.B.) and GM07507 (to J.R.P.). The
authors are grateful to Agnieszka Kubica for help with
data analysis.
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retina, light, superior, dependence, rat, colliculus, innervation
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