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.

Horseradish peroxidase was injected intracellularly into single, physiologically-identified X- and Y-cell geniculocortical axons projecting to area 17 of the cat. This injection anterogradely labeled the axon terminal fields in cortex and retrogradely labeled the somata of these same axons in laminae A and A1 of the lateral geniculate nucleus (LGN). The laminar projections of 21 X- and 15 Y-cell axons were analyzed. For these, the laminar terminations of ten X- and seven Y-cell axons were also related to their cells' positions in the A-laminae. The terminal fields of X- and Y-cell axons overlapped substantially in layers IV and VI of area 17. Some X-cells terminated mainly in IVb, others mainly in IVa, and still others throughout IVa and IVb. The latter two groups also projected up to 100 micron into lower layer III. Y-cells terminated primarily in layer IVa and projected up to 200 microns into lower layer III. Some also arborized throughout the depth of layer IVb. Both X- and Y-cell axons terminated throughout the depth of layer VI, although more so in the upper half. We found no relationship between the diameter of the parent axon and its sublaminar projection within layer IV. Within layer IV, X-cell axons generally terminated within a single, continuous clump and had surface areas of 0.6 to 0.9 mm2. Axons of Y-cells often terminated in two to three separate clumps, separated by terminal free gaps 400 to 600 micron wide. Their total surface areas, including gaps, were 1.0 to 1.8 mm2, roughly 1.6 times the surface areas of X-cell axons. Despite considerable overlap, Y-cell arbors contained significantly more boutons than did X-cell arbors. The sublaminar projections of the X- and Y-cell axons within layer IV reflected the locations of the cells' somata within the depth of the A-laminae. X-cells located in the dorsal or ventral thirds of the depths of the laminae projected mainly to layer IVa or throughout layer IV in cortex. Those located in the central thirds projected mainly to layer IVb. Y-cells showed a similar positional relationship, but they appeared to follow different rules. Y-cells in the outer thirds of the A-laminae projected mainly to layer IVa; those in the central thirds, in addition, expanded their projections to include layer IVb. In general, larger sized somata in the LGN gave rise to more widely spreading terminal arbors and greater numbers of boutons in cortex than did smaller somata.(ABSTRACT TRUNCATED AT 400 WORDS)

1. The lateral geniculate nucleus is the primary thalamic relay through which retinal signals pass en route to cortex. This relay is gated and can be suppressed by activity among local inhibitory neurons that use gamma-aminobutyric acid (GABA) as a neurotransmitter. In the cat, a major source of this GABAergic inhibition seems to arise from cells of the perigeniculate nucleus, which lies just dorsal to the A-laminae of the lateral geniculate nucleus. However, the morphological characteristics of perigeniculate cells, and particularly the projection patterns of their axons, have never been fully characterized. We thus examined the morphology of these cells: individually by intracellular injection of horseradish peroxidase (HRP) and en masse with the anterograde tracer Phaseolus vulgaris leucoagglutinin (PHAL). 2. We recorded from 12 perigeniculate cells that we impaled and successfully labeled with HRP. These cells exhibited response properties generally consistent with those described previously. They had long response latencies to stimulation of the optic chiasm and relatively large, often diffuse, receptive fields. The visually evoked responses of most of the cells were dominated by one eye. Compared with cells of the lateral geniculate nucleus, perigeniculate cells had large somata (517 +/- 136 microns 2 in cross-sectional area, mean +/- SD), which were fusiform or multipolar in shape, and dendritic arbors that extended a considerable distance (1,095 +/- 167 microns) parallel to the border between the perigeniculate and lateral geniculate nuclei. Terminal arbors of some dendrites were quite complex and beaded. 3. The axons of six perigeniculate cells were labeled sufficiently well to trace and reconstruct over a considerable distance. Each of these axons formed branches that descended to innervate the lateral geniculate nucleus, and this geniculate innervation was exclusively limited to the A-laminae. Terminal boutons within the A-laminae were nearly all en passant, which gave the axons a beaded appearance. Furthermore, branches of five of these six axons provided local innervation of the perigeniculate nucleus, generally within each labeled cell's own dendritic arbor. Three of the cells also exhibited an axon branch that extended medially and caudally away from the soma, but we were unable to trace these axon branches to their targets. 4. Within the lateral geniculate nucleus, each arbor of perigeniculate axons derived from two main components. One was a narrow, sparse medial component that innervated laminae A and A1.(ABSTRACT TRUNCATED AT 400 WORDS)