Synaptic connectivity of a local circuit neurone in lateral geniculate nucleus of the cat

Abstract

Although receptive fields of relay cells in the lateral geniculate nucleus of the cat nearly match those of their retinal afferents, only 10-20% of the synapses on these cells derive from the retina and are excitatory. Many more (30-40%) are inhibitory and largely control the gating of retinogeniculate transmission. These inhibitory synapses derive chiefly from two cell types: intrinsic local circuit neurones and cells in the adjacent perigeniculate nucleus. It has been difficult to study the functional organization of these inhibitory pathways; most efforts have relied on indirect approaches. Here we describe the use of direct techniques to study a local circuit neurone by iontophoresing horseradish peroxidase (HRP) into it, which completely labels the soma and processes of cells for subsequent light- and electron microscopic analysis. Although the response properties of the labelled cell are virtually indistinguishable from those of many relay cells, its morphology is typical of 'class 3' neurones (see Fig. 1 legend), which are widely believed to be interneurones (but see ref. 12). Here, we refer to the cell as a 'local circuit neurone', which allows for the possibility of a projection axon, rather than as an 'interneurone', a term that commonly excludes a projection axon. We find that the labelled cell has a myelinated axon, but that the axon loses its myelin within 50 microns of the soma and has not yet been traced further. The dendrites of the labelled cell possess presynaptic terminals that act as intrinsic sources of inhibition on geniculate relay cells. We also characterize other morphological aspects of this inhibitory circuitry.

Spatially distinct actions of metabotropic glutamate receptor activation in dorsal lateral geniculate nucleus

“…We demonstrate that DHPG application to proximal but not distal dendrites produces long-lasting GABA A receptor-mediated inhibition in thalamocortical neurons. Our physiological evidence is supported by anatomic evidence suggesting the presence of triads formed between retinal axon, interneuron dendrites, and thalamocortical dendrites on proximal dendrites of thalamocortical neurons (Hamos et al 1985;Wilson 1989). The proximity of the F2 terminals with retinogeniculate afferents position this mGluR 5 -mediated increase in inhibition to regulate/modulate the magnitude of excitations via the retinogeniculate pathway.…”

“…Local dLGN inhibitory interneurons are unique in that they give rise to two distinct types of output: axonal and dendritic (Famiglietti and Peters 1972;Guillery 1969;Hamos et al 1985;Montero 1986;Ralston 1971). The conventional axonal output of interneurons forms both axodendritic and axosomatic inhibitory synapses onto thalamocortical neurons and are referred to as F1 terminals.…”

Functional Synaptic Contacts by Intranuclear Axon Collaterals of Thalamic Relay Neurons

“…2). Every one of these cells had morphological characteristics of intralaminar interneurons, including small somata; long, richly branched, axoniform dendrites with terminal boutons; and a dendritic arbor oriented perpendicular to laminar borders (Guillery, 1966;Hamos et al, 1985;Pape and McCormick, 1995). These cells were also physiologically identified by their robust depolarizing sag in response to hyperpolarizing current pulses, which seems to result from evoking the hyperpolarizationactivated cation conductance (I h ) and the apparent lack of a low threshold calcium spike (Fig.…”

Metabotropic Glutamate Receptors Differentially Regulate GABAergic Inhibition in Thalamus

“…The specific neuronal subtypes were distinguished by electrophysiological and morphological properties (Fig. 1C) (Hamos et al, 1985;Pape and McCormick, 1995;Williams et al, 1996;Govindaiah and Cox, 2006b). sIPSCs were recorded from dLGN relay neurons using voltage-clamp recording techniques with a holding potential of 0 mV and cesium-containing pipette solution to attenuate postsynaptic actions of mGluR activation (Cox et al, 1998;Cox and Sherman, 2000).…”

“…In the visual system, GABA-containing inhibitory interneurons in the dorsal lateral geniculate nucleus (dLGN) innervate thalamocortical relay neurons by classical axodendritic synapses (F1 terminals) and dendrodendritic synapses (F2 terminals) (Guillery, 1969;Ralston, 1971;Famiglietti and Peters, 1972;Hamos et al, 1985;Montero, 1986). F2 terminals are usually involved in "triadic" arrangements in which retinogeniculate fibers provide monosynaptic excitatory inputs onto the thalamocortical relay neuron dendrites as well as F2 terminals (see Fig.…”