Synaptic patterns in the dorsal lateral geniculate nucleus of the monkey

Summary Synaptic junctions are found in all parts of the nucleus, being almost as densely distributed between cell laminae as within these laminae.In addition to the six classical cell laminae, two thin intercalated laminae have been found which lie on each side of lamina 1. These laminae contain small neurons embedded in a zone of small neural processes and many axo-axonal synapses occur there.Three types of axon form synapses in all cell laminae and have been called RLP, RSD and F axons. RLP axons have large terminals which contain loosely packed round synaptic vesicles, RSD axons have small terminals which contain closely packed round vesicles and F axons have terminals intermediate in size containing many flattened vesicles.RLP axons are identified as retinogeniculate fibers. Their terminals are confined to the cell laminae, where they form filamentous contacts upon large dendrites and asymmetrical regular synaptic contacts (with a thin postsynaptic opacity) upon large dendrites and F axons. RSD axons terminate within the cellular laminae and also between them. They form asymmetrical regular synaptic contacts on small dendrites and on F axons. F axons, which also occur throughout the nucleus, form symmetrical regular contacts upon all portions of the geniculate neurons and with other F axons. At axo-axonal junctions the F axon is always postsynaptic.Supported by Grant R 01 NB 06662 from the USPHS and by funds of the Neurological Sciences Group of the Medical Research Council of Canada. Most of the observations were made while R. W. Guillery was a visiting professor in the Department of Physiology at the University of Montreal. We thank the Department of Physiology for their support and Mr. K. Watkins, Mrs. E. Langer and Mrs. B. Yelk for their skillful technical assistance.     

A multi-compartment model for interneurons in the dorsal lateral geniculate nucleus

GABAergic interneurons (INs) in the dorsal lateral geniculate nucleus (dLGN) shape the information flow from retina to cortex, presumably by controlling the number of visually evoked spikes in geniculate thalamocortical (TC) neurons, and refining their receptive field. The INs exhibit a rich variety of firing patterns: Depolarizing current injections to the soma may induce tonic firing, periodic bursting or an initial burst followed by tonic spiking, sometimes with prominent spike-time adaptation. When released from hyperpolarization, some INs elicit rebound bursts, while others return more passively to the resting potential. A full mechanistic understanding that explains the function of the dLGN on the basis of neuronal morphology, physiology and circuitry is currently lacking. One way to approach such an understanding is by developing a detailed mathematical model of the involved cells and their interactions. Limitations of the previous models for the INs of the dLGN region prevent an accurate representation of the conceptual framework needed to understand the computational properties of this region. We here present a detailed compartmental model of INs using, for the first time, a morphological reconstruction and a set of active dendritic conductances constrained by experimental somatic recordings from INs under several different current-clamp conditions. The model makes a number of experimentally testable predictions about the role of specific mechanisms for the firing properties observed in these neurons. In addition to accounting for the significant features of all experimental traces, it quantitatively reproduces the experimental recordings of the action-potential- firing frequency as a function of injected current. We show how and why relative differences in conductance values, rather than differences in ion channel composition, could account for the distinct differences between the responses observed in two different neurons, suggesting that INs may be individually tuned to optimize network operation under different input conditions.     

Cytoplasmic organelles in neurons of the dorsal lateral geniculate nucleus of aged rats

The ultrastructural characteristics of the neurons containing complex convolutions have been studied in the dorsal lateral geniculate nucleus of the 31-month-old rat. Neurons were seen to contain oval or round dense bodies which were surrounded by a nuclear membrane and granular endoplasmic reticulum. Their perikarya showed rarely clusters of pleomorphic and small clear vesicles intermingled with a few larger vesicles of dense material. Dendrites occasionally exhibited intermediate forms between laminated bodies and complex convolutions. The significance of these features has been discussed.     

Dense cored vesicles in presynaptic profiles of the rabbit dorsal lateral geniculate nucleus

We are carrying out a study about the synaptic relations between identified synaptic profiles in the dorsal lateral geniculate nucleus (dLGN) of the rabbit. Here, the types of synaptic vesicle containing profiles of the dLGN are described. There are presynaptic large profiles containing round vesicles and pale mitochondria (RLP terminals) and small profiles that contain round vesicles and dark mitochondria (RSD terminals) which respectively arise from the retina and the visual cortex. Another type of presynaptic profile contains elliptical vesicles (F-boutons) which can be subdivided according to their cytoplasmic content. These F-boutons arise from dLGN interneurons. We have found different sized vesicles that have a dense core within RLP, and F terminals and a possible RSD terminal. The significance of the coexistance of pale and dense cored vesicles in the presynaptic profiles of the rabbit dLGN is discussed.     

Abnormal functional organization in the dorsal lateral geniculate nucleus of mice lacking the beta 2 subunit of the nicotinic acetylcholine receptor

Spontaneous activity patterns in the developing retina appear important for the functional organization of the visual system. We show here that an absence of early retinal waves in mice lacking the beta2 subunit of the nicotinic acetylcholine receptor (nAChR) is associated with both gain and loss of functional organization in the dorsal lateral geniculate nucleus (dLGN). Anatomical studies show normal gross retinotopy in the beta2(-/-) dLGN but suggest reduced topographic precision in the retinogeniculate projection. Physiological recordings reveal normal topography in the dorsoventral visual axis but a lack of fine-scale mapping in the nasotemporal visual plane. In contrast, unlike wild-type mice, on- and off-center cells in the beta2(-/-) dLGN are spatially segregated. The presence of the beta2 subunit of the nAChR in the CNS is therefore important for normal functional organization in the retinogeniculate projection.     

The organization of synaptic interconnections in the laminae of the dorsal lateral geniculate nucleus of the cat

Summary Four axon types occur in the lateral geniculate nucleus. Two contain vesicles with mainly round profiles and these are distinguished from each other by their size, the appearance of their contents and by the types of contact they make. The larger RLP axons are interpreted as retinogeniculate and the smaller RSD axons as corticogeniculate fibers. The other two axon types contain many irregular or flattened vesicles and these F axons are regarded as two types of intrageniculate fiber.In laminae A and A 1 encapsulated synaptic zones form around grape-like dendritic appendages. These zones contain all axon types, but RSD axons are rare. Interstitial zones lie between the encapsulated zones and contain synapses formed by many RSD axons, some F and few RLP axons. The interstitial zones continue into the central interlaminar nucleus which forms a narrow band containing no encapsulated zones and few RLP axons. Lamina B contains relatively small RLP axons, very many RSD axons and only a few small encapsulated zones.Axosomatic junctions are rare throughout the nucleus. Axo-axonal junctions occur in all laminae but mostly in the encapsulated zones; the postsynaptic element is always an F axon, RLP or RSD axons generally form the presynaptic element.Supported by Grant NB 06662 from the USPHS. The skillful technical assistance given by Mrs. E. Langer during the course of this work is gratefully acknowledged.     

A quantitative study of synaptic interconnections in the dorsal lateral geniculate nucleus of the cat

Summary 2,700 synaptic contacts have been classified according to criteria described in an accompanying paper and the results summarized in tabular form. Only about 20% of the synaptic contacts in laminae A and A1 are formed by axons identifiable as retinogeniculate fibers. About 1/4 of these retinogeniculate synapses are axo-axonal. Approximately 45% of the contacts in these laminae are formed by axons tentatively identifiable as corticogeniculate fibers; about 35% by presumed intrageniculate fibers. Close to one half of the synapses occur in encapsulated synaptic zones, where grapelike dendritic appendages are related mainly to intrageniculate and retinogeniculate axons, and about half lie in interstitial zones, where corticogeniculate and some intrageniculate axons contact distal dendritic segments.Regions of the nucleus receiving from peripheral parts of the retina have relatively more corticogeniculate synapses, and have fewer intrageniculate synapses in the encapsulated zones than do regions receiving from the central parts of the retina.Most of the tissue in lamina B resembles the interstitial zones of laminae A and A1 and over 2/3 of the contacts in lamina B may prove to be corticogeniculate. The retinogeniculate fibers in this lamina are associated with relatively few other axons in simple, small encapsulated zones.Supported by Grant NB 06662 from the USPHS. The skillful technical assistance given by Mrs. E. Langer during the course of this work is gratefully acknowledged.     

Role of calcineurin in activity-dependent pattern formation in the dorsal lateral geniculate nucleus of the ferret

In the retinogeniculate pathway of the ferret, in addition to the separation of the inputs from the two eyes to form eye-specific layers, there is also an anatomical segregation of the terminal arbors of on-center retinal ganglion cells from the terminal arbors of off-center retinal ganglion cell axons to form on/off sublaminae. Sublamination normally occurs during postnatal weeks 3-4 and requires the activity of retinal afferents, N-methyl-D-aspartate receptors, nitric oxide synthase, and a target of nitric oxide, cyclic guanosine monophosphate. Calcineurin is a calcium/calmodulin dependent serine, threonine protein phosphatase suggested to mediate NMDA-receptor dependent synaptic plasticity in the hippocampus. We have examined whether calcineurin plays a role during on/off sublamination in the dorsal lateral geniculate nucleus (dLGN) of the ferret. Immunohistochemistry showed that calcineurin expression is transiently up-regulated in dLGN cells and neuropil during the period of on/off sublamination. A functional role for calcineurin during sublamination was investigated by blocking the enzyme locally via intracranial infusion of FK506. Treatment with FK506 during postnatal weeks 3-4 disrupted the appearance of sublaminae. These results suggest that calcineurin may play a role during this process of activity-dependent pattern formation in the visual pathway.     

The ventral lateral geniculate nucleus,pars lateralis of the rat

Summary The synaptic organization of the pars lateralis portion of the ventral lateral geniculate nucleus is similar to that of other thalamic nuclei. There are four types of synaptic knobs (RL, RS, F1, F2). RL knobs are large and irregularly shaped, contain round synaptic vesicles and make multiple asymmetrical junctions. They are found primarily in synaptic islands making contact with gemmules, spines, small dendrites, and other synaptic profiles containing pleiomorphic synaptic vesicles (F2). Smaller RS knobs contain round vesicles and make asymmetrical junctions with the same type of elements as RL knobs, with the exception of the F2 profiles, but are seldom found in synaptic islands. F1 knobs contain flattened synaptic vesicles and form symmetrical junctions with F2 knobs, gemmules, spines, and small-medium dendrites in synaptic islands, throughout the neuropil, and on the proximal dendrites and soma of the largest type of neuron. F2 knobs are irregularly shaped, contain pleiomorphic synaptic vesicles and make symmetrical junctions primarily with gemmules and spines in synaptic islands. They are postsynaptic to RL and F1 knobs. Occipital decortication indicates that cortical terminals are of the RS type. Bilateral enucleation indicates that retinal terminals are of both the RL and RS type. The large amount of geographic overlap of retinal and cortical terminals on gemmules, spines, and small dendrites found in the neuropil outside of synaptic islands logically would maximize axonal sprouting between these two sources.We would like to thank Mr. Peter Rossetti for his excellent technical assistance on a major portion of this project, Ms. Judith Strauss for photographic assistance, and Ms. Nancy Wood for typing. Supported by grants NS 10579, NS 08724, 5 S01 RR 05402, and 2 T01 GM 00326     

Fine structure of synapses in the dorsal nucleus of the lateral geniculate body of normal and blinded rats

Summary Degenerating boutons, observed from 2 to 60 days after eye enucleation, displayed decreased plasma membrane density, increased axoplasmic density, and enlarged mitochondria with deformed cristae when compared with boutons from normal animals. There was also a loss of synaptic plasma membrane specialization and the boutons abnormally indented contiguous dendrites. The number and appearance of synaptic vesicles in some degenerating boutons were notably altered. Phagocytosis of boutons in most instances appeared to be accomplished by astrocytes. When degeneration was first apparent in some boutons, the subsynaptic organelle in the adjacent dendritic cytoplasm was enlarged, somewhat less dense and was associated with small granular and circular profiles. Subsynaptic organelles in experimental animals were absent from contiguities between dendrites and other cell processes, except in a few instances when only small portions of boutons remained at their synaptic sites, suggesting that the organelles disappeared when boutons had been completely phagocytized.Degenerating myelinated axons, observed from 2 to 300 days after enucleation, exhibited the same triad of features as degenerating boutons. They appeared to be phagocytized in most instances by dense glial processes, presumably oligodendrocytic, which were normally situated between the axon and its myelin sheath and were related to the inner mesaxon.This investigation was supported by U.S.P.H.S. Training Grants Nos. 2 T1 GM 202 T1 CA 505506, and 2RO 1 AM 368806.The author expresses his appreciation to Dr. A. J. Ladman for acquainting him with the techniques used in the study and to Dr. R. J. Barrnett for valuable criticism of this report. Gratitude is also extended to Mr. E. Z. Rutkowski for making the drawing.     

Neuronal types in the lateral geniculate nucleus of man

Summary Nerve cell types of the lateral geniculate body of man were investigated with the use of a transparent Golgi technique that allows study of not only the cell processes but also the pigment deposits. Three types of neurons have been distinguished:Type-I neurons are medium-to large-sized multipolar nerve cells with radiating dendrites. Dendritic excrescences can often be encountered close to the main branching points. Type-I neurons comprise a variety of forms and have a wide range of dendritic features. Since all intermediate forms can be encountered as well, it appears inadequate to subdivide this neuronal type. One pole of the cell body contains numerous large vacuolated lipofuscin granules, which stain weakly with aldehyde fuchsin.Type-II and type-III neurons are small cells with few, sparsely branching and extended dendrites devoid of spines. In Golgi preparations they cannot be distinguished from each other. Pigment preparations reveal that the majority of these cells contains small and intensely stained lipofuscin granules within their cell bodies (type II), whereas a small number of them remains devoid of any pigment (type III). Intermediate forms do not occur.     

Stereological study of the synaptic profiles belonging to interneurons in the dorsal lateral geniculate nucleus of the rabbit.

This study is concerned with some characteristics of the interneurons belonging to the dLGN (dorsal Lateral Geniculate Nucleus) of the rabbit. The work deals with the distribution of such cells in the alpha E sector of the nucleus and their F1 and F2 presynaptic contacts. The F1 and the F2 profiles are present in all three of the alpha E zones studied. The F1 profiles are significantly more numerous in the upper zone (57 +/- 2 profiles per 10(4) microns2 of section) and the middle zone (59 +/- 3 profiles per 10(4) microns2 of section) than in the lower one (41 +/- 2 profiles per 10(4) microns2 of section). The F2 profiles are more abundant in the alpha E sector than the F1 ones are, particularly in the lower zone, where F2 profiles (104 +/- 4 profiles per 10(4) microns2 of section) are not only significantly more numerous than F1 profiles but also more abundant than the F2 profiles in the middle zone (84 +/- 3 profiles per 10(4) microns2 of section) and upper zone (88 +/- 2 profiles per 10(4) microns2 of section). These results and their comments reveal diverse density of the element distribution from the dorsal to the ventral part of the alpha E sector as well as the possible relationship or independence from the extranuclear afferent inputs.     

Synaptic organization in the lateral geniculate nucleus of the monkey

Summary The synaptic organization in the lateral geniculate nucleus of the monkey has been studied by electron microscopy.The axon terminals in the lateral geniculate nucleus can be identified by the synaptic vesicles that they contain and by the specialized contacts that they make with adjacent neural processes. Two types of axon terminal have been recognized. The first type is relatively large (from 3–20 ) and contains relatively pale mitochondria, a great many vesicles and, in normal material, a small bundle of neurofilaments. These terminals have been called LP terminals. The second type is smaller (1–3 ), contains darker mitochondria, synaptic vesicles, and no neurofilaments. These have been called SD terminals.Both types of terminal make specialized axo-somatic and axo-dendritic synaptic contacts, but the axo-somatic contacts are relatively rare. In addition the LP terminals frequently make specialized contacts with the SD terminals, that is, axo-axonal contacts, and at these contacts the asymmetry of the membranes is such that the LP terminal must be regarded as pre-synaptic to the SD terminal.The majority of the synaptic contacts are identical to those that have been described previously (Gray, 1959 and 1963a) but, in addition, a new type of contact has been found. This is characterized by neurofilaments that lie close to the post-synaptic membrane, and by an irregular post-synaptic thickening. Such filamentous contacts have been found only where an LP terminal contacts a dendrite or a soma.The degeneration that follows removal of one eye demonstrates that the LP terminals are terminals of optic nerve fibres. The origin of the SD terminals is not known.The glial cells often form thin lamellae around the neural processes and tend to isolate synaptic complexes. These lamellae occasionally show a complex concentric organization similar to that of myelin.It is a pleasure to thank Prof. J. Z. Young for advice and encouragement and Dr. E. G. Gray for the considerable help he has given us. Dr. J. L. de C. Downer gave us much help with the care of the animals and with the operations. We also wish to thank Mr. K. Watkins for technical assistance and Mr. S. Waterman for the photography.     

Role of calcineurin in activity‐dependent pattern formation in the dorsal lateral geniculate nucleus of the ferret

In the retinogeniculate pathway of the ferret, in addition to the separation of the inputs from the two eyes to form eye‐specific layers, there is also an anatomical segregation of the terminal arbors of on‐center retinal ganglion cells from the terminal arbors of off‐center retinal ganglion cell axons to form on/off sublaminae. Sublamination normally occurs during postnatal weeks 3–4 and requires the activity of retinal afferents, N‐methyl‐D‐aspartate receptors, nitric oxide synthase, and a target of nitric oxide, cyclic guanosine monophosphate. Calcineurin is a calcium/calmodulin dependent serine, threonine protein phosphatase suggested to mediate NMDA‐receptor dependent synaptic plasticity in the hippocampus. We have examined whether calcineurin plays a role during on/off sublamination in the dorsal lateral geniculate nucleus (dLGN) of the ferret. Immunohistochemistry showed that calcineurin expression is transiently up‐regulated in dLGN cells and neuropil during the period of on/off sublamination. A functional role for calcineurin during sublamination was investigated by blocking the enzyme locally via intracranial infusion of FK506. Treatment with FK506 during postnatal weeks 3–4 disrupted the appearance of sublaminae. These results suggest that calcineurin may play a role during this process of activity‐dependent pattern formation in the visual pathway. © 2003 Wiley Periodicals, Inc. J Neurobiol 56: 153–162, 2003