The relationship between pyramidal cell morphology and efferent target was investigated in layer 6 of cat primary visual cortex (area 17). Layer 6 has 2 projections, one to the lateral geniculate nucleus (LGN) and another to the visual claustrum. The cells of origin of each projection were identified by retrograde transport of fluorescent latex microspheres. The labeled cells were visualized in brain slices prepared from area 17, using an epifluorescence compound microscope modified for intracellular recording. Individual retrogradely labeled cells were penetrated and intracellularly stained with Lucifer yellow to visualize the patterns of axons and dendrites associated with each projection. The neurons that give rise to the 2 projections had very different patterns of dendrites and local axonal collaterals, but the patterns within each group were highly stereotyped. The differences between their axonal collaterals were particularly dramatic. Claustrum projecting cells had fine, horizontally directed collaterals that arborized exclusively in layer 6 and lower layer 5. Most LGN projecting cells had virtually no horizontal arborization in layer 6. Instead, they sent widespread collaterals vertically, which arborized extensively in layer 4. The apical dendrites of the 2 groups also differed markedly. Claustrum projecting cells had apical dendrites reaching to layer 1, with branches in layer 5 only, while LGN projecting cells never had an apical dendrite reaching higher than layer 3, with side branches in layers 5 and 4. Therefore, each efferent target must receive inputs from neurons whose synaptic connections within area 17 are significantly different from those of neurons projecting to other targets. This further suggests that distinct visual response properties should be associated with each projection. In addition to the claustrum and LGN projecting cells, about 20% of layer 6 pyramidal neurons lacked an efferent axon. Morphologically, most resembled LGN projecting neurons, but a few had characteristics of claustrum projecting cells. These neurons may represent cells that either failed to make an efferent connection or cells that lost an efferent axon during development. Their frequency suggests that such intrinsic, presumably excitatory, neurons may play a significant role in cortical processing.
In the cerebral cortex, the plant lectin Vicia villosa (VVA) selectively stains the surfaces of nonpyramidal neurons. This lectin binds specifically to alpha- and beta-linked N-acetylgalactosamine (GalNac). VVA-reactive carbohydrate is highly concentrated in layer 4 of the primary visual cortex of the cat, where it is associated exclusively with GABAergic local circuit neurons. We have studied this neuronal subset with intracellular electrophysiological recording and dye marking to identify the particular cell types expressing surface GalNac. Five different types of local circuit neurons were stained intracellularly (N = 45), but only 2 types, the columnar basket and large neurogliaform cells, were also labeled by the lectin (N = 19/45). Lectin negative types included small basket, chandelier, and large bitufted cells (26/45). Spiny stellate and pyramidal neurons were also lectin negative. Electrophysiological recordings revealed differences in the duration of action potentials in smooth versus spiny stellates but no differences between lectin-positive or -negative types. A biochemical analysis of cortical glycoproteins by SDS-PAGE and lectin blotting revealed multiple bands containing GalNac enriched in membrane fractions. These carbohydrate-containing molecules may be part of a biochemical mechanism for linking together cells with common functional properties.
In cat striate cortex, patchy horizontal axonal projections link columns of similar orientation specificity. To assess the physiological correlates of such clustered projections, a new multisite stimulation technique was used to functionally map the pattern of horizontal synaptic inputs onto single layer 2/3 cells within tangential slices of developing ferret visual cortex. Twenty-four separate sets of horizontal fibers were stimulated within a 1200 microns strip of cortex, while evoked synaptic responses were recorded using whole-cell patch methods. For most cells, input maps demonstrated the presence of clustered horizontal connections in which multiple strong and weak synaptic responses were alternately evoked across the stimulated cortical region. Recordings from up to nine cells in a single slice revealed that patterns of synaptic input were closely correlated for cells in close proximity, and that this correlation decreased with distance, with no correlation at distances greater than 500 microns. To determine whether these physiological results were consistent with the known anatomical linkage of iso-orientation columns by clustered horizontal connections, mathematical analysis and computer simulations were performed upon orientation tuning maps obtained from optical imaging of activity-dependent intrinsic signals in mature ferret visual cortex. Optical imaging revealed an organization of iso-orientation domains consisting of broad regions of cortex across which orientation preference smoothly varied, together with "orientation centers" around which orientation preference was arranged in a pinwheel manner. The distribution of synaptic connections between different cortical sites was simulated by a model of functionally linked iso- orientation columns. Simulated synaptic input maps, generated by the same stimulation and recording arrangements used in our experimental protocol, accurately reproduced the observed patterns of clustered inputs onto experimentally recorded cells. These results indicate that even at the time of eye opening, prior to extensive visual experience, most cells receive patterns of synaptic inputs consistent with a clustered organization of horizontal connections that functionally link iso-orientation columns.
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