Ventral lateral geniculate nucleus projects to the dorsal lateral geniculate nucleus in the cat

The lamina C3 of the dorsal lateral geniculate nucleus of the cat does not receive retinal projections but instead receives visual information from the small subpopulation of W-type ganglion cells via the upper substratum of the stratum griseum superficiale of the superior colliculus. We herein report a projection from the lateral division of the ventral lateral geniculate nucleus into the lamina C3 of the dorsal lateral geniculate nucleus. As the lateral division receives projections from the contralateral retina and the ipsilateral upper stratum griseum superficiale of the superior colliculus, we suggest that these regions make up a small cell type W-cell neuronal network that provides visual information to layer I of the striate cortex via the lamina C3.     

Synaptic development of the mouse dorsal lateral geniculate nucleus

The dorsal lateral geniculate nucleus (dLGN) of the mouse has emerged as a model system in the study of thalamic circuit development. However, there is still a lack of information regarding how and when various types of retinal and nonretinal synapses develop. We examined the synaptic organization of the developing mouse dLGN in the common pigmented C57/BL6 strain, by recording the synaptic responses evoked by electrical stimulation of optic tract axons, and by investigating the ultrastructure of identified synapses. At early postnatal ages (<P12), optic tract evoked responses were primarily excitatory. The full complement of inhibitory responses did not emerge until after eye opening (>P14), when optic tract stimulation routinely evoked an excitatory postsynaptic potential/inhibitory postsynaptic potential (EPSP/IPSP) sequence, with the latter having both a GABA_A and GABA_B component. Electrophysiological and ultrastructural observations were consistent. At P7, many synapses were present, but synaptic profiles lacked the ultrastructural features characteristic of the adult dLGN, and little γ‐aminobutyric acid (GABA) could be detected by using immunocytochemical techniques. In contrast, by P14, GABA staining was robust, mature synaptic profiles of retinal and nonretinal origin were easily distinguished, and the size and proportion of synaptic contacts were similar to those of the adult. The emergence of nonretinal synapses coincides with pruning of retinogeniculate connections, and the transition of retinal activity from spontaneous to visually driven. These results indicate that the synaptic architecture of the mouse dLGN is similar to that of other higher mammals, and thus provides further support for its use as a model system for visual system development. J. Comp. Neurol. 518:622–635, 2010. © 2009 Wiley‐Liss, Inc.     

Synaptology of retinal terminals in the dorsal lateral geniculate nucleus of the cat

We have made a fine structural investigation of the synaptic patterns made by axon terminals of retinal ganglion cells in the dorsal lateral geniculate nucleus of the cat. We compared the retinal input to dendritic processes that bear clusters of large appendages with the retinal input to relatively smooth dendritic segments that have only a few isolated spines. The study was restricted to the portion of laminae A and A1 that receive central visual field input. We were able to completely reconstruct 33 individual terminal boutons from long series of consecutive thin sections. Retinal terminals that were presynaptic to dendritic appendages tended to occupy the central position in the complex synaptic zones of geniculate fine structure called glomeruli. These terminals were surrounded by significantly more profiles than retinal terminals that were presynaptic to dendritic stems and averaged twice as many synaptic contacts per terminal bouton. The retinal input to dentritic appendages was heavily involved in a specific synaptic pattern called the triadic arrangement while retinal input to dendritic stems was only lightly involved in triads. Dendritic appendages in triads received greater synaptic input from profiles with flattened vesicles than did the dendritic stems that were found in triads.     

Y retinal terminals contact interneurons in the cat dorsal lateral geniculate nucleus

One of the largest influences on dorsal lateral geniculate nucleus (dLGN) activity comes from interneurons, which use the neurotransmitter gamma-aminobutyric acid (GABA). It is well established that X retinogeniculate terminals contact interneurons and thalamocortical cells in complex synaptic arrangements known as glomeruli. However, there is little anatomical evidence for the involvement of dLGN interneurons in the Y pathway. To determine whether Y retinogeniculate axons contact interneurons, we injected the superior colliculus (SC) with biotinylated dextran amine (BDA) to backfill retinal axons, which also project to the SC. Within the A lamina of the dLGN, this BDA labeling allowed us to distinguish Y retinogeniculate axons from X retinogeniculate axons, which do not project to the SC. In BDA-labeled tissue prepared for electron microscopic analysis, we subsequently used postembedding immunocytochemical staining for GABA to distinguish interneurons from thalamocortical cells. We found that the majority of profiles postsynaptic to Y retinal axons were GABA-negative dendrites of thalamocortical cells (117/200 or 58.5%). The remainder (83/200 or 41.5%) were GABA-positive dendrites, many of which contained vesicles (59/200 or 29.5%). Thus, Y retinogeniculate axons do contact interneurons. However, these contacts differed from X retinogeniculate axons, in that triadic arrangements were rare. This indicates that the X and Y pathways participate in unique circuitries but that interneurons are involved in the modulation of both pathways.     

Reduced retinal activity increases GFAP immunoreactivity in rat lateral geniculate nucleus

Dynamic regulation of astrocytic processes by the electrical activity of local neurons has been previously described in chick cochlear nucleus. The present study extends this observation by showing that astrocytes in the rat lateral geniculate nucleus (LGN) also increase their immunoreactivity for glial fibrillary acidic protein (GFAP) soon after deprivation of afferent visual neuronal activity. Within 6 h of enucleation, which eliminates a major source of afferent input to the contralateral LGN, GFAP immunoreactivity increases relative to the ipsilateral LGN. A similar increase in GFAP immunoreactivity can be induced by intraocular injections of tetrodotoxin, demonstrating that a reversible manipulation of optic nerve electrical activity is sufficient to regulate LGN astrocytes. This rapid response to activity deprivation is less dramatic than the gliotic reaction observed 3 weeks following deafferentation, by which time afferent terminals have degenerated. These results support the notion that regulation of astrocytic processes by neural activity may play an important role in activity-dependent synaptic regulations in the various sensory systems of vertebrates.     

The influence of retinal afferents upon the development of layers in the dorsal lateral geniculate nucleus of mustelids

The extent to which the development of a normal laminated lateral geniculate nucleus depends upon retinal afferents has been studied in normal and albino ferrets and in mink. Removal of all retinal afferents before they invade the nucleus (28 days in utero) or before they establish distinct monocular terminal fields (newborn, approximately 41 days post-conception) produces a nucleus that is smaller than normal and poorly separated from the adjacent perigeniculate and medial interlaminar nuclei. However, the nucleus is wedge-shaped, resembling a normal adult nucleus, in which a broad medial binocular segment is distinguishable from a narrower lateral monocular segment. There is a normal mediolateral gradient of cell sizes and some signs of a laminar differentiation, cells next to the optic tract being morphologically distinguishable from cells near the optic radiation, but no cell-free interlaminar zones are formed. The development of a monocularly innervated nucleus depends on the size of the surviving retinal input. In normally pigmented ferrets or mink the crossed retinofugal component is larger than the uncrossed component. In the monocular animals one sees essentially a monocular set of geniculate layers on each side, with an appropriate asymmetry. Each nucleus can be regarded as representing the survival of those layers which would have been innervated by the good eye, together with some additional geniculate territory that appears to be added to the surviving layers as retinogeniculate axons occupy territory normally innervated by the other eye. The crossed component of an albino ferret is abnormally large and the monocularly innervated contralateral nucleus is almost like that of a normal albino. There is a full complement of geniculate layers and interlaminar zones, which appears to develop without any binocular interactions. The ipsilateral retinogeniculate component of albinos is extremely small. In the monocular albino animals it forms discontinuous terminal patches, leaving sectors of the poorly differentiated nucleus uninnervated. These results show that in geniculate development there is a limited interaction between the two sets of retinal afferents. Each set plays a well defined and distinctive role, and one can replace the other to a limited extent only.     

The absence of retinal input disrupts the development of cholinergic brainstem projections in the mouse dorsal lateral geniculate nucleus

Background

The dorsal lateral geniculate nucleus (dLGN) of the mouse has become a model system for understanding thalamic circuit assembly. While the development of retinal projections to dLGN has been a topic of extensive inquiry, how and when nonretinal projections innervate this nucleus remains largely unexplored. In this study, we examined the development of a major nonretinal projection to dLGN, the ascending input arising from cholinergic neurons of the brainstem. To visualize these projections, we used a transgenic mouse line that expresses red fluorescent protein exclusively in cholinergic neurons. To assess whether retinal input regulates the timing and pattern of cholinergic innervation of dLGN, we utilized the math5-null (math5^?/?) mouse, which lacks retinofugal projections due to a failure of retinal ganglion cell differentiation.

Results

Cholinergic brainstem innervation of dLGN began at the end of the first postnatal week, increased steadily with age, and reached an adult-like pattern by the end of the first postnatal month. The absence of retinal input led to a disruption in the trajectory, rate, and pattern of cholinergic innervation of dLGN. Anatomical tracing experiments reveal these disruptions were linked to cholinergic projections from parabigeminal nucleus, which normally traverse and reach dLGN through the optic tract.

Conclusions

The late postnatal arrival of cholinergic projections to dLGN and their regulation by retinal signaling provides additional support for the existence of a conserved developmental plan whereby retinal input regulates the timing and sequencing of nonretinal projections to dLGN.

     

Role of retinal afferents in regulating growth and shape of the lateral geniculate nucleus

Segregated binocular maps in the dorsal lateral geniculate nucleus (LGN) develop from a stage where they initially overlap. Sophisticated computational models have been used to describe the dynamics of three-dimensional LGN shape changes that play a role in segregation. These models have revealed specific nuclear growth vectors associated with the process of ocular segregation in the LGN (Williams and Jeffery [2001] J Comp Neurol 430:332-342.). In this study, we use similar techniques to determine whether retinal innervation contributes to the dynamics of shape maturation in the ferret LGN. In this animal, 90% of the retinal innervation of the mature LGN comes from the contralateral eye. If one eye is removed before segregation, the projection from the remaining eye remains diffuse and nuclear growth is stunted. Here, we quantify this effect and show that removing the contralateral projection before segregation has a profound impact on LGN size but changes its ultimate shape by only 12%. The impact on shape on the other side of the brain where the ipsilateral projection is removed, which accounts for only 10% of its innervation in maturity, is less than 2%. Hence, retinal innervation plays a minor role in determining mature LGN shape. Although in both hemispheres, the ultimate shape of the nucleus is close to normal, removal of the larger projection disrupts normal growth vectors, with almost none being present in the 5 days after enucleation, when the normal nucleus expands markedly. Hence, the effect of enucleation is to delay shape maturation. Growth vectors absent after removal of the smaller projection are mainly confined to those in what would be the binocular region.     

Dependence of cytochrome oxidase activity in the rat lateral geniculate nucleus on retinal innervation

Patterns of cytochrome oxidase (CO) activity were examined histochemically in the dorsal lateral geniculate nucleus (LGNd) and retina of pigmented rats. CO staining was not uniform and was distributed in a pattern similar to that of retinal afferents. Portions of the LGNd receiving an exclusively crossed projection were moderately reactive whereas regions receiving an uncrossed or overlapping crossed and uncrossed projection were darkly reactive. The dependence of oxidative metabolic activity in the LGNd on retinal innervation was verified in animals with unilateral enucleation. In adults, chronic monocular enucleation led to a decrease in CO staining in portions of the LGNd deprived of retinal input; in animals enucleated at birth, normal patterns of CO reactivity failed to develop and both LGNds had a more uniform pattern of moderate CO staining. Most neurons in the ganglion cell layer of the retina were moderately reactive for CO. However, there were approximately 3,000 darkly reactive cells, most of which appear to be ganglion cells. The darkly reactive cells were more numerous in the peripheral temporal retina. The laminar pattern of CO staining in the retina was similar to that described previously for carnivores and primates. The most reactive laminae were the inner and outer plexiform layers and the photoreceptor inner segments. Within the inner plexiform layer, sublamina a was more darkly stained than sublamina b. These results suggest that the physiological properties of crossed and uncrossed visual pathways in rats are functionally dissimilar at the level of both the retina and the LGNd.     

Distribution of morphologically different retinal axon terminals in the hamster dorsal lateral geniculate nucleus

Afferent terminal arbors in the hamster LGBd were labelled with horseradish peroxidase (HRP) implanted into the optic tract. Three morphologically distinct terminal types, each with a different regional distribution, were observed. Type R1 terminals are large, ovoid swellings and are predominantly distributed medially within the nucleus. Type R2 terminals are very small, clustered varicosities and are distributed laterally and ventrally. Type R3 terminals are medium in size and their distribution overlaps with that of Type R1 and R2 terminals.     

Sizes of neurons in the primate lateral geniculate nucleus during normal development

Measurements of cell area have been made in the lateral geniculate nuclei (LGNs) of 18 normal rhesus monkeys aged from 8 days to fully adult. There is much less variability between individual animals than had been thought from measurements of undeprived cells in experimental animals following visual deprivation. It is therefore possible to make reliable comparisons of cell size between different animals. There is no change in size of cells in the parvocellular laminae between 8 days of age and adulthood, although cells in the magnocellular laminae grow a little. In the primate, unlike the cat, the period of maximum sensitivity to visual deprivation does not correspond to a period of rapid cell growth in the LGN.     

Cholecystokinin-like immunoreactive retinal ganglion cells project to the ventral lateral geniculate nucleus in pigeons

A subpopulation of retinal ganglion cells projecting to the pigeon ventral lateral geniculate nucleus was shown to contain cholecystokinin-like immunoreactivity. These ganglion cells were mainly distributed in the peripheral retina, and their somata sizes were medium to large (14-23 microns). Taken together with previous findings, these results indicate that the retinal input to the ventral geniculate is chemically heterogeneous.     

Prenatal development of retinal ganglion cell axons: segregation into eye-specific layers within the cat's lateral geniculate nucleus

The morphological changes in individual retinal ganglion cell axons associated with the formation of the eye-specific layers in the dorsal lateral geniculate nucleus (LGN) were studied during the prenatal development of the cat's visual system. Previous work has shown that the pattern of segregated eye inputs found in the adult arises from an immature state in which inputs from the two eyes are intermixed within the nucleus (Shatz, 1983). Here, this developmental process is examined at its fundamental unit of connectivity--the individual retinal ganglion cell axon. To do so, an in vitro method was used to label fetal cat optic tract axons with HRP at various times during development between embryonic day 38 (E38) and postnatal day 2 (P2) (gestation = 65 d). The results presented here are based on reconstructions of 172 axons. During the initial period of intermixing (E38-43), axons are relatively simple in morphology. Many axons studied at the earliest ages (E38) end in growth cones and have very few branches along the main axon trunk as they traverse the nucleus. By E43, the number of side branches given off along the main axon trunk has increased and most axons also have a simple terminal arbor. Over the next 2 weeks (E43-55), the majority of axons are studded with side branches and the terminal arbor is well defined. Then, between E55 and birth, axons lose their side branches and the eye-specific layers appear. By birth, nearly all axons have a smooth trunk and an elaborate terminal arbor restricted to the LGN layer appropriate to the eye of axon origin. When the number of side branches per axon was quantified, the time course of appearance and subsequent loss of side branches was found to parallel the time course of the initial intermixing of inputs and subsequent reduction in territory shared by the two eyes as determined from previous intraocular injection experiments. Our results also showed that the side branches along each axon were located primarily within LGN territory destined to be occupied by the other eye. Thus, the side branches are likely to represent a morphological substrate for the intermixing of inputs from the two eyes. These observations suggest that the segregation of eye input to the LGN involves two fundamental and simultaneous events. One event is the remodeling of the branching pattern along the length of the main axon trunk so that the side branches present early on are eliminated and the main axon trunk becomes smooth.(ABSTRACT TRUNCATED AT 400 WORDS)     

The development of unit activity in the lateral geniculate nucleus of the kitten

The spontaneous unit activity in the lateral geniculate nucleus of 15 kittens has been analyzed in terms of the sleep-wake state. Lateral geniculate units in animals ranging from 2 days to 5 weeks of age were recorded under chronic conditions by means of a hydraulically movable glass micropipet. During the first postnatal month, the mean frequency of firing increased progressively in the awake state and in paradoxical sleep but was not modified in quiet or slow wave sleep. However, as early as the third postnatal week, the pattern of modulation of the frequency of unit discharge in response to changes in state reached an organization close to that seen in the adult cat. The most dramatic alteration in the cellular discharge configuration was represented by the introduction of the “burst-pause” pattern in slow wave sleep. Serial interspike interval distributions demonstrated the appearance of this pattern at the end of the second week. The organization of unit firing in the 1-month-old animal was qualitatively similar to that in the adult, though quantitatively less intense. The pattern of development of unit firing is discussed in light of the appearance of other important developmental features such as cortical synchronization, ponto-geniculo-occipital spikes, and maturation of certain monamine-containing cells in the central nervous system. Some structural and neurochemical factors in development are mentioned that may be responsible for the ontogenetic organization of unit discharges in the lateral geniculate nucleus.     

Elimination of neurons from the rhesus monkey's lateral geniculate nucleus during development

The timing, magnitude, and spatial distribution of neuron elimination was studied in the dorsal lateral geniculate nucleus of 57 rhesus monkeys (Macaca mulatta) ranging in age from the 48th day of gestation to maturity. Normal and degenerating cells were counted in Nissl-stained sections by using video-enhanced differential interference contrast optics and video-overlay microscopy. Before embryonic day 60 (E60), the geniculate nucleus contains 2,200,000 +/- 100,000 neurons. Roughly 800,000 of these neurons are eliminated over a 40- to 50-day period spanning the middle third of gestation. Neurons are lost at an average rate of 300 an hour between E48 and E60, and at an average rate of 800 an hour between E60 and E100. Very few neurons are lost after E100, and as early as E103 the population has fallen to the adult average of 1,400,000 +/- 90,000. Degenerating neurons are far more common in the magnocellular part of the nucleus than in the parvicellular part. In 20 of 29 cases, the number of neurons is greater on the right than on the left side. The right-left asymmetry averages about 8.5% and the difference is statistically significant (phi 2 = 38, p less than .001). The period of cell death occurs before the emergence of cell layers in the geniculate nucleus, before the establishment of geniculocortical connections, and before the formation of ocular dominance columns (Rakic, '76). Most important, the depletion of neurons in the geniculate nucleus begins long before the depletion of retinal axons. The number of geniculate neurons is probably a key factor controlling the number of the retinal cells that survive to maturity.     

The organization of retinal maps within the dorsal and ventral lateral geniculate nuclei of the rabbit

The cytoarchitectonic subdivisions in the rabbit's dorsal and ventral lateral geniculate nuclei have been related to the several retinal maps that can be defined in terms of the distribution of retinal axons within these nuclei. Destruction of different retinal sectors was combined with intravitreal injections of ³H-proline, so that the distribution of fiber degeneration and autoradiographic label in the geniculate nuclei could be used to define the retinal maps in each nucleus, and to compare the two nuclei with each other. The two nuclei show surprisingly similar patterns of organization. Each is made up of a laminated alpha sector that curves around a relatively cell-sparse beta sector. Two morphologically distinct layers of each alpha sector receive contralateral retinal afferents and between these there is a small region in receipt of ipsilateral afferents. In each nucleus, the lines of projection that represent single points in visual space pass perpendicular to the layers of the alpha sector and continue an almost straight course into the beta sector. Quantitative comparisons of the retinal maps show that the relative volumes devoted to the representation of segments of the visual field are approximately the same in the two nuclei.     

Plasticity in the chick ventral lateral geniculate nucleus

The chick ventral lateral geniculate nucleus (GLv) receives topographically corresponding projections from the retina and optic tectum. Tectal lesions produced on the day of hatching removed the tectogeniculate input to the GLv region corresponding to the tectal lesion and also severed some retinotectal axons. Following a survival period of 3 to 10 weeks, a patch of augmented retinogeniculate projection was noted in the GLv segment that corresponds topographically to the damaged area of the tectum. Changing the site of the tectal lesion led to changes in the locus of heavy retinal projection to the GLv predictable from topographic maps. Nuclei which received retinal but not tectal projections did not appear to have regions of augmented retinal termination nor did nuclei which received tectal but not retinal innervation. It is unlikely that the increased retinogeniculate termination is due to rerouting of growing retinotectal axons since the chick retinofugal pathway is well established by the time of hatching. Furthermore, there was no evidence of a projection from the ipsilateral eye to the affected GLv. On the basis of these light microscopic studies, it would appear that retinogeniculate terminals have sprouted in the GLv and that competition for terminal space, conservation of terminal space, proximity, and perhaps other factors are necessary for the augmented projection to occur.     

The dorsal lateral geniculate nucleus of macropodid marsupials: cytoarchitecture and retinal projections

The anatomy of the dorsal lateral geniculate nucleus (LGd) is described in five macropodid species, including two rat kangaroos (bettong and potoroo), two wallabies (pademelon and tammar), and the large grey kangaroo. The distribution of retinal terminals in the LGd was examined following intraocular injections of tritiated amino acids. There are considerable differences in both LGd cytoarchitecture and the patterns of retinal terminations among the five species. Cytoarchitecture in the bettong LGd is relatively simple, displaying a minimal regional differentiation. In contrast, the potoroo LGd is quite complex and displays several well-defined cell laminae, each of which is associated with input from a single eye. Both rat kangaroos display the same basic pattern of retinal termination with three bands of terminals from the contralateral eye and four from the ipsilateral eye. The bands are less sharply defined in the bettong, in which terminals from each eye overlap to a greater extent than is seen in the potoroo. The wallabies and kangaroos display a more complex LGd architecture and patterning of retinal terminal bands. Bilateral retinal projections within the same LGd lamina are unusual in these large macropodids. The number of terminal bands reaches ten in the grey kangaroo--four from the contralateral eye and six from the ipsilateral eye. The pademelon LGd is unusual in that it shows intraspecies variation with some animals displaying five ipsilateral terminal bands and others only four. The results are discussed in comparison with the patterns of LGd organisation observed in other mammalian lines, placental and marsupial. We conclude that LGd lamination and the segregation of retinal inputs to the LGd in marsupials are likely to be the result of evolutionary factors which differ from those which have produced ocular segregation and complex lamination in several lines of placental mammals.