Is there a geniculohypothalamic tract in primates? A comparative immunohistochemical study in the circadian system of strepsirhine and haplorhine species.

In rodents, the circadian rhythm generated by the hypothalamic suprachiasmatic nucleus (SCN) is modulated by two types of phenomena: photic phase-shifts, mediated by the retinohypothalamic pathway and non-photic phase-shifts mediated by the projection of the intergeniculate leaflet (IGL) to the SCN which contains the neuropeptide Y (NPY). In primates, the retinohypothalamic pathway has been well-demonstrated but very little is known about the geniculohypothalamic tract. This prompted us to study NPY immunoreactivity in both the SCN and the IGL in species representative of the three main primate lineages: prosimians (Microcebus), New World monkeys (Callithrix) and Old World monkeys (Macacca). In species studied, we found a region in the pregeniculate nucleus containing both NPY immunopositive cells and substance P immunopositive fibres that we identified as the IGL. During evolution, this structure has moved from a ventral to a dorsomedial position relative to the adjacent dorsal lateral geniculate nucleus. By contrast, NPY-IP fibres in the SCN are dense in prosimians, but are sparse or absent in other primate species. We suggest that either the geniculohypothalamic projection is absent in higher primates as is the case in humans, or is absent in diurnal mammals, or contains a different peptide, or that NPY immunoreactivity varies according to other parameters.

Unusual pattern of retinogeniculate projections in the controversial primate Tarsius.

Studies of simian and prosimian primates have demonstrated a remarkable interspecific constancy in the pattern of innervation of the magnocellular and parvocellular layers of the dorsal lateral geniculate nucleus (dLGN) by retinal afferents. The characteristic organization of this nucleus in primates, as well as its apparent phylogenetic stability, have led to the proposal that the distinct laminar arrangement of the dLGN is one of the diagnostic characters that define the Order Primates. Here, we describe the distribution of retinal afferents to the dLGN of Tarsius, the single contemporary member of an ancient lineage of primates. In this genus, the more superficial layer of the dLGN receives projections from the ipsilateral eye, a unique situation among the members of the Order Primates. This observation adds support to the proposal that Tarsius does not share a more recent common ancestry with simians as compared with lemuriform and lorisiform primates.

The suprachiasmatic nucleus in the sheep: retinal projections and cytoarchitectural organization.

The retinal innervation, cytoarchitectural, and immunohistochemical organization of the suprachiasmatic nucleus (SCN) was studied in the domestic sheep. The SCN is a large elongated nucleus extending rostrocaudally for roughly 3 mm in the hypothalamus. The morphology is unusual in that the rostral part of the nucleus extends out of the main mass of the hypothalamus onto the dorsal aspect of the optic chiasm. Following intraocular injection of wheat-germ agglutinin-horseradish peroxidase or tritiated amino acids, anterograde label is distributed throughout the SCN. Retinal innervation of the SCN is bilaterally symmetric or predominantly ipsilateral. Quantitative image analysis demonstrates that, although the amount of autoradiographic label is greatest in the ventral and central parts of the nucleus, density varies progressively between different regions. In addition to the SCN, retinal fibers are also seen in the medial preoptic area, the anterior and lateral hypothalamic area, the dorsomedial hypothalamus, the retrochiasmatic area, and the basal telencephalon. Whereas the SCN can be identified using several techniques, complete delineation of the nucleus requires combined tract tracing, cytoarchitectural, and histochemical criteria. Compared with the surrounding hypothalamic regions, the SCN contains smaller, more densely packed neurons, and is largely devoid of myelinated fibers. Cell soma sizes are smaller in the ventral SCN than in the dorsal or lateral parts, but an obvious regional transition is lacking. Using Nissl, myelin, acetylcholinesterase, and cytochrome oxidase staining, the SCN can be clearly distinguished in the rostral and medial regions, but is less differentiated toward the caudal pole. Immunohistochemical demonstration of several neuropeptides shows that the neurochemical organization of the sheep SCN is heterogeneous, but that it lacks a distinct compartmental organization. Populations of different neuropeptide-containing cells are found throughout the nucleus, although perikarya positive for vasoactive intestinal polypeptide and fibers labeled for methionine-enkephalin are predominant ventrally; neurophysin-immunoreactive cells are more prominent in the dorsal region and toward the caudal pole. The results suggest that the intrinsic organization of the sheep SCN is characterized by gradual regional transitions between different zones.

Neuroanatomical pathways linking vision and olfaction in mammals.

Retinal projections to several telencephalic structures have been demonstrated in a wide range of mammalian species following intraocular injections of tritiated amino acids and cholera toxin subunit-B conjugated to horseradish peroxidase. Since these regions are also innervated by olfactory fibers, we investigated the distribution of convergent projections using simultaneous injections of different anterograde tracers in the eye and olfactory bulbs. Convergent projections from the retina and from the olfactory bulbs were observed in the piriform cortex, olfactory tubercle, the cortical region of the medial amygdala, lateral hypothalamus, and the bed nucleus of the stria terminalis. A few retinal fibers also invade the nucleus of the lateral olfactory tract, the bed nucleus of the accessory olfactory bulb and the diagonal band of Broca. Injections of retrograde tracers in the medial amygdala, the bed nucleus or the lateral hypothalamus shows that the visuo-olfactory convergence mainly involves projections originating from the accessory olfactory bulb, and to a lesser extent from the ventromedial region of the main olfactory bulb. Fewer than 20 retinotelencephalic ganglion cells were identified in the retina, mainly located contralateral to the injection site. Ganglion cells were medium sized and possessed two long slender opposing dendrites. These retinal and olfactory projections could provide an anatomical substrate for the modulation of gonadotropin hormone levels and the olfactory influence on light mediated rhythms related to reproductive physiology.

Visual system of a naturally microphthalmic mammal: the blind mole rat, Spalax ehrenbergi.

Retinal projections and visual thalamo-cortical connections were studied in the subterranean mole rat, belonging to the superspecies Spalax ehrenbergi, by anterograde and retrograde tracing techniques. Quantitative image analysis was used to estimate the relative density and distribution of retinal input to different primary visual nuclei. The visual system of Spalax presents a mosaic of both regressive and progressive morphological features. Following intraocular injections of horseradish peroxidase conjugates, the retina was found to project bilaterally to all visual structures described as receiving retinal afferents in non-fossorial rodents. Structures involved in form analysis and visually guided behaviors are reduced in size by more than 90%, receive a sparse retinal innervation, and are cytoarchitecturally poorly differentiated. The dorsal lateral geniculate nucleus, as defined by cyto- and myelo-architecture, cytochrome oxidase, and acetylcholinesterase distribution as well as by afferent and efferent connections, consists of a narrow sheet 3-5 neurons thick, in the dorsal thalamus. Connections with visual cortex are topographically organized but multiple cortical injections result in widespread and overlapping distributions of geniculate neurons, thus indicating that the cortical map of visual space is imprecise. The superficial layers of the superior colliculus are collapsed to a single layer, and the diffuse ipsilateral distribution of retinal afferents also suggests a lack of precise retinotopic relations. In the pretectum, both the olivary pretectal nucleus and the nucleus of the optic tract could be identified as receiving ipsilateral and contralateral retinal projections. The ventral lateral geniculate nucleus is also bilaterally innervated, but distinct subdivisions of this nucleus or the intergeniculate leaflet could not be distinguished. The retina sends a sparse projection to the dorsal and lateral terminal nuclei of the accessory optic system. The medial terminal nucleus is not present. In contrast to the above, structures of the "non-image forming" visual pathway involved in photoperiodic perception are well developed in Spalax. The suprachiasmatic nucleus receives a bilateral projection from the retina and the absolute size, cytoarchitecture, density, and distribution of retinal afferents in Spalax are comparable with those of other rodents. A relatively hypertrophied retinal projection is observed in the bed nucleus of the stria terminalis. Other regions which receive sparse visual input include the lateral and anterior hypothalamic areas, the retrochiasmatic region, the sub-paraventricular zone, the paraventricular hypothalamic nucleus, the anteroventral and anterodorsal nuclei, the lateral habenula, the mediodorsal nucleus, and the basal telencephalon.(ABSTRACT TRUNCATED AT 400 WORDS)

Ocular regression conceals adaptive progression of the visual system in a blind subterranean mammal.

The mole rat, Spalax ehrenberghi, is an extreme example of natural visual degeneration in mammals: visual pathways are regressed and incomplete, and the absence of visual cortical potentials or an overt behavioural response to light have led to the conclusion that Spalax is completely blind. But structural and molecular investigations of the atrophied, subcutaneous eye suggest a functional role for the retina in light perception, and entrainment of circadian locomotor and thermoregulatory rhythms by ambient light demonstrates a capacity for photoperiodic detection. We report here that severe regression of thalamic and tectal structures involved in form and motion perception is coupled to a selective hypertrophy of structures subserving photoperiodic functions. As an alternative to the prevalent view that ocular regression results from negative or nonselective evolutionary processes, the differential reduction and expansion of visual structures in Spalax can be explained as an adaptive response to the underground environment.

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

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.

Retinal projection to mammalian telencephalon.

Retinal projections were studied in species from 8 orders of mammals using anterograde tracing techniques. The olfactory tubercle of basal telencephalon receives a projection from the retina in all animals. In all species the course of labelled fibers is similar and the terminal distribution of label along the internal border of the granular cell layer is restricted to the mediocaudal region of the tubercle. These shared characteristics suggest that this pathway is a typical mammalian feature, possibly providing for convergence of visual and chemosensory information in telencephalon.