Retinohypothalamic pathway: A breach in the law of Newton-Müller-Gudden?

doi:10.1016/0006-8993(89)90737-3

Brain Research

Volume 488, Issues 1–2, 29 May 1989, Pages 390-397

https://doi.org/10.1016/0006-8993(89)90737-3 Get rights and content

Abstract

Theories of binocular vision originally imagined by Newton provided the foundation for subsequent investigations of the visual system by early anatomists and physiologists. These studies led to the widely accepted concept that degree of optic fiber decussation in the chiasm is inversely related to frontal orientation of the optical axes of the eyes (law of Newton-Müller-Gudden). A survey of 23 species from 11 mammalian orders demonstrates that, in contrast to other visual pathways, the retinohypothalamic projection does not obey this general principle. In further contradiction, an unexpected finding in primates is the predominance of ipsilateral, rather than contralateral, retinal input to the suprachiasmatic nucleus. This unusual organization underlines the functional and evolutionary specificities of this ‘non-image forming’ visual pathway.

References (34)

CavalcanteL.A. et al.
Development of retino-hypothalamic and accessory optic projections in the opossum
Brain Research
(1978)
CavalcanteL.A. et al.
Hypothalamic, tectal and accessory optic projections in the opossum
Brain Research
(1975)
FrostD.O. et al.
Postnatal development of retinal projections in Syrian hamster: a study using autoradiographic and anterograde degeneration techniques
Neuroscience
(1979)
JohnsonR.F. et al.
Retinohypothalamic projections in the hamster and the rat demonstrated using cholera toxin
Brain Research
(1988)
KitaH. et al.
An anterograde HRP study of retinal projections to the hypothalamus in the rat
Brain Res. Bull.
(1982)
MayR. et al.
The suprachiasmatic nuclei and retinohypothalamic tract in the western spoted skunk
Brain Research
(1985)
MooreR.Y.
Retinohypothalamic projection in mammals: a comparative study
Brain Research
(1973)
RepérantJ. et al.
The retinofugal pathways in a primitive actinopterygian, the condrostean Acipenser güdenstädti. An experimental study using degeneration, radioautographic and HRP methods
Brain Research
(1982)
ReppertS.M. et al.
Effects of damage to the suprachiasmatic area of the anterior hypothalamus on the daily suprachiasmatic area of the anterior hypothalamus on the daily melatonin and cortisol rhythms in the rhesus monkey
J. Neurosci.
(1981)
ThorpeP.A.
The presence of a retinohypothalamic projection in the ferret
Brain Research
(1975)

TiggesJ. et al.

An autoradiographic investigation of the subcortical visual system in chimpanzee

J. Comp. Neurol.

(1977)

VesselkinN.P. et al.

The retinofugal and retinopetal systems in Lampetra fluviatilis. An experimental study using radioautographic and HRP methods

Brain Research

(1980)

WallsG.L.

The Vertebrate Eye and its Adaptive Radiation (1942)

CotterJ.R. et al.

Retinofugal projections of non echolocating and echolocating bats

J. Comp. Neurol.

(1979)

CowanW.M. et al.

The autoradigraphic demonstration of axonal connections in the central nervous system

Brain Research

(1972)

GroosG.A.

The neurophysiology of the mammalian suprachiasmatic nucleus and its visual afferents

HendricksonA. et al.

An autoradiogfaphic and electron microscopic study of retino-hypothalamic connections

Z. Zellforsch.

(1972)

Cited by (56)

Neuroanatomy of the extended circadian rhythm system
2013, Experimental Neurology
The suprachiasmatic nucleus (SCN), site of the primary clock in the circadian rhythm system, has three major afferent connections. The most important consists of a retinohypothalamic projection through which photic information, received by classical rod/cone photoreceptors and intrinsically photoreceptive retinal ganglion cells, gains access to the clock. This information influences phase and period of circadian rhythms. The two other robust afferent projections are the median raphe serotonergic pathway and the geniculohypothalamic (GHT), NPY-containing pathway from the thalamic intergeniculate leaflet (IGL). Beyond this simple framework, the number of anatomical routes that could theoretically be involved in rhythm regulation is enormous, with the SCN projecting to 15 regions and being directly innervated by about 35. If multisynaptic afferents to the SCN are included, the number expands to approximately brain 85 areas providing input to the SCN. The IGL, a known contributor to circadian rhythm regulation, has a still greater level of complexity. This nucleus connects abundantly throughout the brain (to approximately 100 regions) by pathways that are largely bilateral and reciprocal. Few of these sites have been evaluated for their contributions to circadian rhythm regulation, although most have a theoretical possibility of doing so via the GHT. The anatomy of IGL connections suggests that one of its functions may be regulation of eye movements during sleep. Together, neural circuits of the SCN and IGL are complex and interconnected. As yet, few have been tested with respect to their involvement in rhythm regulation.
The suprachiasmatic nucleus and the intergeniculate leaflet in the rock cavy (Kerodon rupestris): Retinal projections and immunohistochemical characterization
2010, Brain Research
Citation Excerpt :
A common feature of the SCN of all mammalian species studied is the bilateral innervation from the retina, except for some squirrel species, in which that innervation is described to be exclusively contralateral (Agarwala et al., 1989; Smale et al., 1991). The pattern of the retino-SCN innervation has been described as almost completely contralateral, predominantly ipsilateral, or with almost complete bilateral symmetry (Magnin et al., 1989; see comments in Costa et al., 1999). The functional significance of variability in the pattern of RHT innervation in the SCN remains unknown.
In this study, two circadian related centers, the suprachiasmatic nucleus (SCN) and the intergeniculate leaflet (IGL) were evaluated in respect to their cytoarchitecture, retinal afferents and chemical content of major cells and axon terminals in the rock cavy (Kerodon rupestris), a Brazilian rodent species. The rock cavy SCN is innervated in its ventral portion by terminals from the predominantly contralateral retina. It also contains vasopressin, vasoactive intestinal polypeptide and glutamic acid decarboxilase immunoreactive cell bodies and neuropeptide Y, serotonin and enkephalin immunopositive fibers and terminals and is marked by intense glial fibrillary acidic protein immunoreactivity. The IGL receives a predominantly contralateral retinal projection, contains neuropeptide Y and nitric oxide synthase-producing neurons and enkephalin immunopositive terminals and is characterized by dense GFAP immunoreactivity. This is the first report examining the neural circadian system in a crepuscular rodent species for which circadian properties have been described. The results are discussed comparing with what has been described for other species and in the context of the functional significance of these centers.
Immunocytochemical characterization of the pregeniculate nucleus and distribution of retinal and neuropeptide Y terminals in the suprachiasmatic nucleus of the Cebus monkey
2009, Journal of Chemical Neuroanatomy
Circadian rhythms generated by the suprachiasmatic nucleus (SCN) are modulated by photic and non-photic stimuli. In rodents, direct photic stimuli reach the SCN mainly through the retinohypothalamic tract (RHT), whereas indirect photic stimuli are mainly conveyed by the geniculohypothalamic tract (GHT). In rodents, retinal cells form a pathway that reaches the intergeniculate leaflet (IGL) where they establish synapses with neurons that express neuropeptide Y (NPY), hence forming the GHT projecting to the SCN. In contrast to the RHT, which has been well described in primates, data regarding the presence or absence of the IGL and GHT in primates are contradictory. Some studies have suggested that an area of the pregeniculate nucleus (PGN) of primates might be homologous to the IGL of rodents, but additional anatomical and functional studies on primate species are necessary to confirm this hypothesis. Therefore, this study investigated the main histochemical characteristics of the PGN and the possible existence of the GHT in the SCN of the primate Cebus, comparing the distribution of NPY immunoreactivity, serotonin (5-HT) immunoreactivity and retinal terminal fibers in these two structures. The results show that a collection of cell bodies containing NPY and serotonergic immunoreactivity and retinal innervations are present within a zone that might be homologous to the IGL of rodents. The SCN also receives dense retinal innervations and we observed an atypical distribution of NPY- and 5-HT-immunoreactive fibers without regionalization in the ventral part of the nucleus as described for other species. These data may reflect morphological differences in the structures involved in the regulation of circadian rhythms among species and support the hypothesis that the GHT is present in some higher primates (diurnal animals).
Segregated hemispheric pathways through the optic chiasm distinguish primates from rodents
2008, Neuroscience
Citation Excerpt :
All of the marmoset tissue used in this study was obtained from animals used primarily for other purposes. It came either at postmortem from animals used in unrelated physiology or anatomy studies, or from tissue already processed for a comparative study of the ocular innervation of the suprachiasmatic nucleus (Magnin et al., 1989; Mick et al., 1993). Optic fibers through the nerve and chiasm were stained in eight common marmosets (Callithrix jacchus).
At the optic chiasm retinal fibers either cross the midline, or remain uncrossed. Here we trace hemispheric pathways through the marmoset chiasm and show that fibers from the lateral optic nerve pass directly toward the ipsilateral optic tract without any significant change in fiber order and without approaching the midline, while those from medial regions of the nerve decussate directly. Anterograde labeling from one eye shows that the two hemispheric pathways remain segregated through the proximal nerve and chiasm with the uncrossed confined laterally. Retrograde labeling from the optic tract confirms this. This clearly demonstrates that hemispheric pathways are segregated through the primate chiasm.
Previous chiasmatic studies have been undertaken mainly on rodents and ferrets. In these species there is a major change in fiber order pre-chiasmatically, where crossed and uncrossed fibers mix, reflecting their embryological history when all fibers approach the midline prior to their commitment to innervate either hemisphere. This pattern was thought to be common to placental mammals. In marsupials there is no change in fiber order and uncrossed fibers remain confined laterally through nerve and chiasm, again, reflecting their developmental history when all uncrossed fibers avoid the midline. Recently it has been shown that this distinction is not a true dichotomy between placental mammals and marsupials, as fiber order in tree shrews and humans mirrors the marsupial pattern.
Architectural differences in the mature chiasm probably reflect different developmental mechanisms regulating pathway choice. Our results therefore suggest that both the organization and development of the primate optic chiasm differ markedly from that revealed in rodents and carnivores.
Organization of the circadian system in the subterranean mole rat, Cryptomys hottentotus (Bathyergidae)
2003, Brain Research
The mole rat, Cryptomys hottentotus (Bathyergidae) is a gregarious subterranean rodent, which shows no entrainment to ambient light–dark cycles. The locomotor activity of individuals or of a whole colony, which shows no circadian rhythmicity. Since the lack of both synchronization to light–dark cycle and an endogenous rhythm of locomotor activity could be related to the organization of the circadian system, we have investigated the neuropeptidergic features of the SCN and IGL, and have used pseudorabies viral tracing methods to identify the visual and circadian pathways in this species. The precise topographic distribution of certain neuropeptide populations in the SCN differs from typical rodent pattern of organization and may be correlated with the apparent absence of light entrainment of activity and lack of endogenous rhythmicity. The IGL is highly reduced in size. This structure can nevertheless be identified by the presence of NPY and CALB positive neurons, as well as by a dense network of SP fibers. Viral tracing using intraocular injection of the PRV-Becker and PRV-Bartha strains, leads to differential infection of neurons in circadian and visual structures. With the Bartha strain, infected neurons are principally observed in the SCN, whereas the Becker strain leads primarily to infection of the dLGN and shows an anatomical regression of visual structures. Transsynaptic retrograde infection of the retina contralateral to the injected eye reveals a morphologically homogeneous population, which resemble to retinohypothalamic ganglion cells described in other mammals.
Increased masking response to light after ablation of the visual cortex in mice
2003, Brain Research
Citation Excerpt :
With the inclusion of the present result, enhanced masking by light has now been found after damage to the visual system at three different levels: the retina, the thalamus, and the cortex. An enhanced response to light in an animal with extensive damage to its visual system can be understood if one distinguishes between a classical visual system for image perception and an irradiance detection system for telling night from day [19,10,2,14,8]. An additional assumption is necessary, that there is some interaction between these two systems [16,17].
Mice are known to suppress their wheel running when given a pulse of light in the night (masking response). The amount of suppression can be quantified; the response varies with the level of irradiance used during the light pulse. After ablation of the visual cortex, mice suppressed their activity more than sham-operated controls. In addition, the lesioned animals responded to lower levels of irradiance than controls. It is suggested that the visual cortex is not needed for the suppression of locomotor activity after a light pulse. Nevertheless it exerts an inhibitory influence on the masking response to light mediated by an irradiance detection system. When this inhibition is removed, even though pattern vision is lost, masking responses to ambient level of light are enhanced.

View all citing articles on Scopus

: Supported by grants from INSERM, Ministère de l'Education Nationale and University Claude Bernard (Dept. Biologie Humaine) Lyon.

¹: We thank N. Boyer and S. Beaumont for excellent histological assistance, S. Bello for photography and C. Urquizar for computer programming. We are grateful to J. Kaas for supplying slides of the tree shrew. C. Blakemore, A. Hein and J. Bullier provided helpful criticism of the text.

View full text

Retinohypothalamic pathway: A breach in the law of Newton-Müller-Gudden?

Abstract

Brain Research

Brain Research

Neuroscience

Brain Research

Brain Res. Bull.

Brain Research

Brain Research

Brain Research

J. Neurosci.

Brain Research

J. Comp. Neurol.

Brain Research

Retinofugal projections of non echolocating and echolocating bats

J. Comp. Neurol.

The autoradigraphic demonstration of axonal connections in the central nervous system

Brain Research

The neurophysiology of the mammalian suprachiasmatic nucleus and its visual afferents

An autoradiogfaphic and electron microscopic study of retino-hypothalamic connections

Z. Zellforsch.