close

Вход

Забыли?

вход по аккаунту

?

Light-dependent retinal innervation of the rat superior colliculus.

код для вставкиСкачать
THE ANATOMICAL RECORD 290:341–348 (2007)
Light-Dependent Retinal Innervation of
the Rat Superior Colliculus
J. ROXANNE PRICHARD,1* HILDA S. ARMACANQUI,2 RUTH M. BENCA,3
2
AND MARY BEHAN
1
Behavioral Neuroscience Program, University of St. Thomas, St. Paul, Minnesota
2
Department of Comparative Biosciences, University of Wisconsin, Madison, Wisconsin
3
Department of Psychiatry, University of Wisconsin, Madison, Wisconsin
ABSTRACT
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,
1998).
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
Ó 2007 WILEY-LISS, INC.
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: jrprichard@stthomas.edu
Received 27 July 2005; Accepted 4 January 2007
DOI 10.1002/ar.20424
Published online 23 February 2007 in Wiley InterScience (www.
interscience.wiley.com).
342
PRICHARD ET AL.
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.
MATERIALS AND METHODS
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
guidelines.
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
RETINOCOLLICULAR PROJECTION IN DARK-REARING
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
0.05.
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
343
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).
Observations
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).
RETINOCOLLICULAR PROJECTION IN DARK-REARING
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.
Rearing
condition
LD
LD
LD
LD
DD
DD
DD
DD
Sample
Optical
density
St. Dev.
Lateral
Middle
Medial
All Samples
Lateral
Middle
Medial
All samples
0.852
0.772
0.768
0.807
0.762
0.707
0.778
0.768
0.01
0.03
0.04
0.01
0.07
0.06
0.12
0.02
representative sections from each retina showed no significant differences between rearing groups in the central or peripheral retina (P > 0.05).
DISCUSSION
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
345
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
study.
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).
346
PRICHARD ET AL.
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.
ACKNOWLEDGMENTS
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.
LITERATURE CITED
Akerman CJ, Smyth D, Thompson ID. 2002. Visual experience
before eye-opening and the development of the retinogeniculate
pathway. Neuron 36:869–879.
Angelucci A, Clasca F, Sur M. 1996. Anterograde axonal tracing
with the subunit B of cholera toxin: a highly sensitive immunohistochemical protocol for revealing fine axonal morphology in
adult and neonatal brains. J Neurosci Methods 65:101–112.
Argandona EG, Lafuente JV. 1996. Effects of dark-rearing on the
vascularization of the developmental rat visual cortex. Brain Res
732:43–51.
RETINOCOLLICULAR PROJECTION IN DARK-REARING
Argandona EG, Lafuente JV. 2000. Influence of visual experience
deprivation on the postnatal development of the microvascular
bed in layer IV of the rat visual cortex. Brain Res 855:137–142.
Beckstead RM, Frankfurter A. 1983. A direct projection from the
retina to the intermediate gray layer of the superior colliculus
demonstrated by anterograde transport of horseradish peroxidase
in monkey, cat and rat. Exp Brain Res 52:261–268.
Behan M, Kime NM. 1996. Spatial distribution of tectotectal connections in the cat. In: Norita M, Bando T, Stein BE, editors. Progress in brain research. New York: Elsevier. p 131–142.
Benca RM, Bergmann BM, Leung C, Nummy D, Rechtschaffen A.
1991. Rat strain differences in response to dark pulse triggering
of paradoxical sleep. Physiol Behav 49:83–87.
Benca RM, Gilliland MA, Obermeyer WH. 1998. Effects of lighting
conditions on sleep and wakefulness in albino lewis and pigmented brown Norway rats. Sleep 21:451–460.
Benevento LA, Bakkum BW, Cohen RS. 1995. gamma-Aminobutyric
acid and somatostatin immunoreactivity in the visual cortex of
normal and dark-reared rats. Brain Res 689:172–182.
Binns KE, Salt TE. 1997. Post eye-opening maturation of visual
receptive field diameters in the superior colliculus of normal- and
dark-reared rats. Brain Res Dev Brain Res 99:263–266.
Boka K, Chomsung R, Li J, Bickford ME. 2006. Comparison of the
ultrastructure of cortical and retinal terminals in the rat superior
colliculus. Anat Rec A Discov Mol Cell Evol Biol 288:850–858.
Bronchti G, Rado R, Terkel J, Wollberg Z. 1991. Retinal projections
in the blind mole rat: a WGA-HRP tracing study of a natural
degeneration. Brain Res Dev Brain Res 58:159–170.
Cambras T, Diez-Noguera A. 1991. Evolution of rat motor activity
circadian rhythm under three different light patterns. Physiol
Behav 49:63–68.
Canal-Corretger MM, Vilaplana J, Cambras T, Diet-Noguera A.
2001. Functioning of the rat circadian system is modified by light
applied in critical postnatal days. Am J Physiol Regul Integr
Comp Physiol 280:R1023–1030.
Carman LS, Schneider GE. 1992. Aberrant retinal projections to
midbrain targets mediate spared visual orienting function in
hamsters with neonatal lesions of superior colliculus. Exp Brain
Res 90:92–102.
Caspy T, Babkoff H. 1983. Early prolonged light-deprivation in
hooded rats: deficits in two visual discrimination paradigms. Int J
Psychophysiol 1:83–89.
Chapman B, Godecke I, Bonhoeffer T. 1999. Development of orientation preference in the mammalian visual cortex. J Neurobiol
41:18–24.
Coolen LM, Jansen HT, Goodman RL, Wood RI, Lehman MN. 1999.
A new method for simultaneous demonstration of anterograde
and retrograde connections in the brain: co-injections of biotinylated dextran amine and the beta subunit of cholera toxin. J Neurosci Methods 91:1–8.
Cooper HM, Herbin M, Nevo E. 1993. Visual system of a naturally
microphthalmic mammal: the blind mole rat, Spalax ehrenbergi.
J Comp Neurol 328:313–350.
Czepita D, Reid SN, Daw NW. 1994. Effect of longer periods of dark
rearing on NMDA receptors in cat visual cortex. J Neurophysiol
72:1220–1226.
Dallimore EJ, Cui Q, Beazley LD, Harvey AR. 2002. Postnatal
innervation of the rat superior colliculus by axons of late-born
retinal ganglion cells. Eur J Neurosci 16:1295–1304.
Dean P, Mitchell IJ, Redgrave P. 1988. Responses resembling defensive behaviour produced by microinjection of glutamate into superior colliculus of rats. Neuroscience 24:501–510.
Fagiolini M, Pizzorusso T, Berardi N, Domenici L, Maffei L. 1994.
Functional postnatal development of the rat primary visual cortex
and the role of visual experience: dark rearing and monocular deprivation. Vision Res 34:709–720.
Flandrin JM, Jeannerod M. 1977. Lack of recovery in collicular neurons from the effects of early deprivation or neonatal cortical
lesion in the kitten. Brain Res 120:362–366.
Fleming MD, Benca RM, Behan M. 2006. Retinal projections to the
subcortical visual system in congenic albino and pigmented rats.
Neuroscience 143:895–904.
347
Guenther E, Schmid S, Wheeler-Schilling T, Albach G, Grunder T,
Fauser S, Kohler K. 2004. Developmental plasticity of NMDA receptor function in the retina and the influence of light. FASEB J
18:1433–1435.
Harrington ME. 1997. The ventral lateral geniculate nucleus and
the intergeniculate leaflet: interrelated structures in the visual
and circadian systems. Neurosci Biobehav Rev 21:705–727.
Helms MC, Ozen G, Hall WC. 2004. Organization of the intermediate gray layer of the superior colliculus: I, intrinsic vertical connections. J Neurophysiol 91:1706–1715.
Hoffmann KP, Sherman SM. 1975. Effects of early binocular deprivation on visual input to cat superior colliculus. J Neurophysiol
38:1049–1059.
Hubel DH, Weisel TN. 1963. Receptive fields of cells in striate cortex of very young, visually inexperienced kittens. J Neurophysiol
26:994–1002.
Huerta MF, Harting JK. 1984. The mammalian superior colliculus:
studies of its morphology and connections. In: Vanegas H, editor.
Comparative neurology of the optic tectum. New York: Plenum
Press. p 687–773.
Hunt DL, King B, Kahn DM, Yamoah EN, Shull GE, Krubitzer L.
2005. Aberrant retinal projections in congenitally deaf mice: how
are phenotypic characteristics specified in development and evolution? Anat Rec 287A:1051–1066.
King AJ, Hutchings ME, Moore DR, Blakemore C. 1988. Developmental plasticity in the visual and auditory representations in
the mammalian superior colliculus. Nature 332:73–76.
King SM, Dean P, Redgrave P. 1991. Bypassing the saccadic pulse
generator: possible control of head movement trajectory by rat
superior colliculus. Eur J Neurosci 3:790–801.
King AJ, Carlile S. 1993. Changes induced in the representation of
auditory space in the superior colliculus by rearing ferrets with
binocular eyelid suture. Exp Brain Res 94:444–455.
Kratz KE, Sherman SM, Kalil R. 1979. Lateral geniculate nucleus
in dark-reared cats: loss of Y cells without changes in cell size.
Science 203:1353–1355.
Lee P, Helms MC, Augustine CJ, Hall WC. 1997. Role of intrinsic
circuitry in collicular sensorimotor integration. Proc Natl Acad
Sci USA 94:13299–13304.
Lee P, Hall WC. 2006. An in vitro study of horizontal connections in
the intermediate layer of the superior colliculus. J Neurosci
26:4763–4768.
Lund RD, Bunt AH. 1976. Prenatal development of central optic
pathways in albino rats. J Comp Neurol 165:247–264.
McHaffie JG, Wang S, Walton N, Stein BE, Redgrave P. 2002.
Covariant maturation of nocifensive oral behaviour and c-fos
expression in rat superior colliculus. Neuroscience 109:597–
607.
Miller AM, Miller RB, Obermeyer WH, Behan M, Benca RM. 1999.
The pretectum mediates rapid eye movement sleep regulation by
light. Behav Neurosci 113:755–765.
Morin LP, Blanchard JH. 1998. Interconnections among nuclei of
the subcortical visual shell: the intergeniculate leaflet is a major
constituent of the hamster subcortical visual system. J Comp
Neurol 396:288–309.
Mower GD, Burchfiel JL, Duffy FH. 1981. The effects of dark-rearing on the development and plasticity of the lateral geniculate nucleus. Brain Res 227:418–424.
Obermeyer WH, Benca RM. 1999. REM sleep in response to light
and dark in congenic albino and pigmented F344 rats. Sleep Res
Online 2:83–88.
Paxinos G, Kus L, Ashwell KWS, Watson C. 1999. Chemoarchitectonic atlas of the rat forebrain. San Diego, CA: Academic Press.
Pettit DL, Helms MC, Lee P, Augustine GJ, Hall WC. 1999. Local
excitatory circuits in the intermediate gray layer of the superior
colliculus. J Neurophysiol 81:1424–1427.
Prichard JR, Stoffel RT, Quimby DL, Obermeyer WH, Benca RM,
Behan M. 2002. Fos immunoreactivity in rat subcortical visual shell
in response to illuminance changes. Neuroscience 114:781–793.
Prichard JR, Fahy JL, Obermeyer WH, Behan M, Benca RM. 2004.
Sleep-wakefulness responses to light are shaped by early experience. Behav Neurosci 118:1262–1273.
348
PRICHARD ET AL.
Redgrave P, Dean P, Souki W, Lewis G. 1981. Psychopharmacology
75:198–203.
Redgrave P, Westby GW, Dean P. 1993. Functional architecture of
rodent superior colliculus: relevance of multiple output channels.
Prog Brain Res 95:69–77.
Sahibzada N, Dean P, Redgrave P. 1986. Movements resembling orientation or avoidance elicited by electrical stimulation of the
superior colliculus in rats. J Neurosci 6:723–733.
Saito U, Isa T. 1999. Elctrophysiologic and morphological properties
of neurons in the rat superior colliculus: I, neurons in the intermediate layer. J Neurophysiol 82:754–767.
Saito U, Isa T. 2005. J Neuorphysiol. Organization of interlaminar
interactions in the rat superior colliculus. J Neurophysiol 93:
2898–2907.
Sasaki K, Ino H, Chiba T, Adachi-Usami E. 1999. Light-induced apoptosis in the neonatal mouse retina and superior colliculus.
Invest Ophthalmol Vis Sci 40:3079–3083.
Schiller PH, Stryker M. 1972. Single-unit recording and stimulation
in superior colliculus of the alert rhesus monkey. J Neurophysiol
35:915–924.
Schneider GZ. 1969. Two visual systems. Science 163:895–902.
Sefton AJ, Dreher B. 1995. Visual system. In: Paxinos G, editor.
The rat nervous system. San Diego: Academic Press. p 833–898.
Sherman SM. 1973. Visual field defects in monocularly and binocularly deprived cats. Brain Res 49:25–45.
Sherman SM, Spear PD. 1982. Organization of visual pathways in
normal and visually deprived cats. Physiol Rev 62:738–855.
Stein BE, Clamann HP. 1981. Control of pinna movements and sensorimotor register in cat superior colliculus. Brain Behav Evol 19:180–192.
Stein BE, Meredith MA, Wallace MT. 1993. The visually responsive
neuron and beyond: multisensory integration in cat and monkey.
Prog Brain Res 95:79–90.
Wallace MT, Stein BE. 1997. Development of multisensory neurons
and mulitsensory integration in cat superior colliculus. J Neurosci
17:2429–2944.
Wallace MT, Perrault TJ Jr, Hairston WD, Stein BE. 2004. Visual
experience is necessary for the development of multisensory integration. J Neurosci 24:9580–9584.
Wickelgren-Gordon B. 1972. Some effects of visual deprivation on
the cat superior colliculus. Invest Ophthalmol 11:460–467.
Wiesel TN, Hubel DH. 1965. Extent of recovery from the effects of
visual deprivation in kittens. J Neurophysiol 28:1060–1072.
Withington DJ. 1992. The effect of binocular lid suture on auditory
responses in the guinea-pig superior colliculus. Neurosci Lett
136:53–156.
Zhang J, Yang Z, Wu SM. 2005. Development of cholinergic amacrine cells is visual activity-dependent in the postnatal mouse retina. J Comp Neurol 484:331–343.
Zwiers MP, Van Opstal AJ, Cruysberg JR. 2001. A spatial-hearing
deficit in early-blind humans. J Neurosci 21:1–5.
Документ
Категория
Без категории
Просмотров
0
Размер файла
850 Кб
Теги
retina, light, superior, dependence, rat, colliculus, innervation
1/--страниц
Пожаловаться на содержимое документа