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.     

Brightness contrast effects in monkey lateral geniculate nucleus.

Brightness contrast effects shown by single cells in the macaque's lateral geniculate nucleus were studied with black and white lines of various widths, consisting of either: (1) "simultaneous contrast" stimuli in which the line was produced by luminance changes in the flanking areas or (2) "successive contrast" stimuli in which the line itself changed in luminance. Line widths that gave optimal responses and response magnitudes themselves were similar for the two types of stimulus, except for the widest lines used (2 degrees). Thus, simultaneous brightness contrast is a primary determinant of the response of primate LGN cells but only within 2 degrees of the center of the receptive field. Neural processing up to this level cannot therefore explain the long distance effects of simultaneous brightness contrast in human perception.     

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.     

Single-unit recording in the lateral geniculate nucleus of the awake behaving monkey

In recent years, recording neuronal activity in the awake, behaving primate brain has become established as one of the major tools available to study the neuronal specificity of the initiation and control of various behaviors. Primates have traditionally been used in these studies because of their ability to perform more complex behaviors closely akin to those of humans, a desirable prerequisite since our ultimate aim is to elucidate the neuronal correlates of human behaviors. A wealth of knowledge has accumulated on the sensory and motor systems such as vision, audition, and eye movements. For more demanding behaviors where the main focus has been on attention, recordings in awake primates have begun to yield valuable data on the centers of the brain that are reactive to different attributes of this behavior. As a result, various hypotheses of the origin and distribution of attentional effects have evolved. For instance, visual attentional effects have been described not only in the higher cortical area (V4) but also in areas earlier in the visual pathway which presumably involve a feedback mechanism in the latter region. Here we outline the ways in which we have successfully used these methods to make single-cell recordings in awake macaques to show how certain behavioral paradigms affect neurons of the thalamus (with emphasis on the lateral geniculate nucleus). As we have done with established techniques these methods can be readily adapted to incorporate most behaviors needed to be tested and allow recordings to be made in virtually any part of the brain.     

Origin and dynamics of extraclassical suppression in the lateral geniculate nucleus of the macaque monkey

In addition to the classical, center/surround receptive field of neurons in the lateral geniculate nucleus (LGN), there is an extraclassical, nonlinear surround that can strongly suppress LGN responses. This form of suppression likely plays an important role in adjusting the gain of LGN responses to visual stimuli. We performed experiments in alert and anesthetized macaque monkies to quantify extraclassical suppression in the LGN and determine the roles of feedforward and feedback pathways in the generation of LGN suppression. Results show that suppression is significantly stronger among magnocellular neurons than parvocellular neurons and that suppression arises too quickly for involvement from cortical feedback. Furthermore, the amount of suppression supplied by the retina is not significantly different from that in the LGN. These results indicate that extraclassical suppression in the macaque LGN relies on feedforward mechanisms and suggest that suppression in the cortex likely includes a component established in the retina.     

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.     

Recovery from monocular deprivation in the monkey. II. Reversal of morphological effects in the lateral geniculate nucleus

The cross-sectional area was measured of neurons in the lateral geniculate nucleus (l.g.n.) of monkeys (Erythrocebus patas) subjected to monocular deprivation by unilateral eyelid suture, and of others in which the closed lids had been subsequently opened (either alone, "reopening', or together with closure of the previously open eye, "reverse suture'). Monocular deprivation for the first month of the monkey's life retards l.g.n. cell growth such that neurons in the laminae innervated by the closed eye are about 15% smaller in cross-sectional area than those in normally innervated laminae. This failure of normal growth can be countered by reverse suture for even short periods of time, the size difference between laminae being abolished within 6 days after reverse suture performed at the age of 1 month. Simply reopening the closed eye has little or no effect on l.g.n. neuronal recovery. These morphological results in the l.g.n. correlate closely with studies on the width of ocular dominance "stripes' in layer IVc of the visual cortex of the same animals: the stripes, narrower than normal after monocular deprivation, "expand' with a time course similar to that of l.g.n. cell recovery, as judged by single unit recording and by autoradiography in the cortex after transneuronal transport of labelled tracers injected in an eye.     

Tailoring of variability in the lateral geniculate nucleus of the cat

 Variability is usually considered an unwanted component in a sensory signal, yet the visual system does not seem to filter out the noise. On the contrary, noise is ‘tailored’ to scale with the signal size. We show that this tailoring occurs in the lateral geniculate nucleus, preferentially in X-cells, which are the cells most likely to transmit pattern information. Tailoring the variability to the signal size may be the visual system’s way of providing the right amount of variability for a signal of any magnitude at all times during the computation. Received: 13 November 1995/Accepted in revised form: 20 May 1996     

Parvalbumin,calbindin, and calretinin mark distinct pathways during development of monkey dorsal lateral geniculate nucleus

Immunocyochemical labeling was applied to follow the developmental changes in the calcium-binding proteins parvalbumin (PV), calbindin D28k (CaB), and calretinin (CaR) during fetal and infant development of Macaca monkey dorsal lateral geniculate nucleus (LGN). For all three proteins, LGN cell body and retinal ganglion cell (RGC) axon labeling patterns changed temporally and spatially over development, and many of these were LGN laminar specific. CaR+ and CaB+ cells were present at the youngest age studied, fetal day 55 (F55). After lamination of the LGN occurred between F90 and F115, CaR+ and CaB+ neurons were specific markers for the S, intercalated, and interlaminar layers. Double label immunocytochemistry showed that all CaR+ cells contained CaB, and none contained GABA. CaR+ cell bodies decreased in number soon after birth so that adult LGN contained only a very small number of CaR+ cells. These patterns and cell counts indicated that a downregulation of CaR had occurred in the CaB+ population. Although CaB+ cell density in S and interlaminar zones declined in the adult, cell counts indicated that this is due to dilution of a stable population into a much larger nucleus during development. PV+ cells appeared at F85 only within the putative magnocellular (M) and parvocellular (P) layers, and PV remained a marker for these layers throughout development. Fetal PV cells also contained GABA, indicating that they were LGN interneurons. After birth, GABA−/PV+ cell numbers increased dramatically throughout the whole nucleus so that by the end of the first year, P and M layers were filled with PV+ cells. Their number and size indicated that these were the LGN projection neurons. Beginning at F66, bundles of PV+ axons occupied the anterior-middle LGN and filled the optic tract. Up to F101, PV+ synaptic terminals were restricted to P layers, but after F132 labeling in M layers was heavier than in P layers. Axonal labeling for CaR began at F125. Prenatally CaR+ terminals were present mainly in P layers, whereas by postnatal 9 weeks labeling in M layers much exceeded P layers. Axonal labeling for CaB was present at F132, but CaB+ terminals were observed only after birth with labeling always heavier in M than P layers. By postnatal 9 weeks, PV, CaR, and CaB were colocalized in the same axons and terminals. These experiments indicated that during development and in the adult LGN, both CaR and CaB were markers for the LGN neurons in the S and intercalated pathway. CaR was present transiently while CaB persisted into adulthood. PV was a M and P layer marker first for interneurons and later for projection cells. The complex temporal developmental patterns found in this study suggested that viewing PV, CaB, and CaR simply as calcium-buffering proteins severely underestimates their functional roles during visual system maturation. © 1996 John Wiley & Sons, Inc.     

On the neurons and synapses of the lateral geniculate nucleus of the monkey,and the effects of eye enucleation

Summary Two neuron types are distinguished by electron microscopy in the lateral geniculate nucleus (LGN) of the monkey-a large cell (P cell) interpreted as a geniculostriate relay cell, and a small cell (I cell) interpreted as an inhibitory interneuron. The I cell, distinguished by its small size, infolded nucleus, small mitochondria, cilium and small granular bodies, forms about 10% of the total neuron population. It could not be determined whether this cell has an axon, but its dendrites, which contain aggregates of flattened vesicles, are thought to form a proportion of the F processes, profiles which are post-synaptic to the retinal (RLP) axons and presynaptic to the dendrites of the P cells. The small dark (RSD) axon terminals of unknown origin contact the dendrites of both cell types.After eye enucleation the P cells of the affected laminae of the LGN shrink and partially withdraw their dendrites from the neuropil. By 29 months' survival, they have only a narrow cytoplasmic rim around the nucleus. A necrotic process also occurs, affecting fine dendrites by 22 days and large profiles by 45 days, but it is not clear whether whole cells are destroyed by this process. At 45 days the I cells are commonly seen to form somatodendritic synapses. The appearance of these synapses is interpreted as the result of a withdrawal to the soma of the presynaptic dendrites.It is concluded that the I cells are probably inhibitory interneurons subject to excitation and presynaptic inhibition by the RLP and RSD axons, and a diagram is presented to demonstrate the possible significance of these connections for the transmission of information through the LGN.The author wishes to thank Dr. J. Campos-Ortega for much practical advice.     

Rapid plasticity of visual responses in the adult lateral geniculate nucleus

Compared to the developing visual system, where neuronal plasticity has been well characterized at multiple levels, little is known about plasticity in the adult, particularly within subcortical structures. We made intraocular injections of 2-amino-4-phosphonobutyric acid (APB) in adult cats to block visual responses in On-center retinal ganglion cells and examined the consequences on visual responses in the lateral geniculate nucleus (LGN) of the thalamus. In contrast to current views of retinogeniculate organization, which hold that On-center LGN neurons should become silent with APB, we find that ～50% of On-center neurons rapidly develop Off-center responses. The time course of these emergent responses and the actions of APB in the retina indicate the plasticity occurs within the LGN. These results suggest there is greater divergence of retinogeniculate connections than previously recognized and that functionally silent, nonspecific retinal inputs can serve as a substrate for rapid plasticity in the adult.     

Entrainment of oscillatory neural activity in the cat's lateral geniculate nucleus

Oscillatory neural activity in the frequency range 7–12 Hz is observed in the lateral geniculate nucleus (LGN) of the lightly anesthetized cat. This paper describes a series of experiments in which the interactions between ongoing oscillatory potentials and periodic photic and electrical stimuli are analyzed using frequency domain techniques. The principal results of these experiments are consistent with a model of the neural system as an entrainable oscillator in which ongoing oscillations are suppressed by stimulation at nearby frequencies, but coexist with stimulus frequencies farther away. The physiological interpretation of these results may be closely tied to the role of the LGN as a gating mechanism between retina and cortex.Supported by NIH Training Grant #GM01455 and NSF Grant #ENG-7515736     

The beta sector of the rabbit's dorsal lateral geniculate nucleus

The beta sector of the rabbit's dorsal lateral geniculate nucleus is a small region of nerve cells scattered among the fibres of the geniculocortical pathway. In its topographical relations it resembles the perigeniculate nucleus of carnivores, which contains neurons driven by geniculate and visual cortical neurons and which sends inhibitory fibres back into the geniculate relay. We have traced retinogeniculate, geniculocortical and corticogeniculate pathways in rabbits by using horseradish peroxidase or radioactively labelled proline and have found that the beta sector resembles the perigeniculate nucleus in receiving no direct retinal afferents, sending no efferents to the visual cortex (V-I), and receiving afferents from the visual cortex. The corticogeniculate afferents are organized so that the visual field map in the beta sector and the main part of the lateral geniculate relays are aligned, as are the maps in the cat's perigeniculate nucleus and the main part of the geniculate relay of carnivores. Electron microscopical studies show similar types of axon terminals in the rabbit and the cat for the main part of the geniculate relay on the one hand and for the beta sector and the perigeniculate nucleus on the other. Earlier observations that the proportion of putative inhibitory terminals (F-type terminals) is lower in the rabbit's than the cat's geniculate region are confirmed. A major difference between the beta sector and the perigeniculate nucleus has been revealed by immunohistochemical staining for GABA. Whereas almost all of the cat's perigeniculate cells appear to be GABAergic, the proportion in the beta sector is much lower, and not significantly different from that found in the main part of the rabbit's geniculate relay. It is concluded that the beta sector shares many of the organizational features of the perigeniculate nucleus. A common developmental origin seems probable, but the functional differences remain to be explored.     

Saccadic eye movements modulate visual responses in the lateral geniculate nucleus

We studied the effects of saccadic eye movements on visual signaling in the primate lateral geniculate nucleus (LGN), the earliest stage of central visual processing. Visual responses were probed with spatially uniform flickering stimuli, so that retinal processing was uninfluenced by eye movements. Nonetheless, saccades had diverse effects, altering not only response strength but also the temporal and chromatic properties of the receptive field. Of these changes, the most prominent was a biphasic modulation of response strength, weak suppression followed by strong enhancement. Saccadic modulation was widespread, and affected both of the major processing streams in the LGN. Our results demonstrate that during natural viewing, thalamic response properties can vary dramatically, even over the course of a single fixation.