An intracellular analysis of geniculo‐cortical connectivity in area 17 of the cat.

Abstract

The latencies of excitatory and inhibitory post-synaptic potentials (e.p.s.p. and i.p.s.p.) evoked by electrical stimulation of afferents from the lateral geniculate nucleus were recorded in neurons of area 17 of the cat visual cortex. After application of an extrapolation procedure to compensate for the conduction time of the afferent axons, a histogram of latencies formed 3 distinct peaks. Potentials in each of these were interpreted as being mediated by mono-, di- and trisynaptic pathways. Characteristic laminar differences in the extracellular field potentials evoked from the lateral geniculate nucleus (l.g.n.) and in the antidromic activation of neurons from the l.g.n. and superior colliculus were used to determine the laminar position of recorded neurons. It was found that within a given layer, all cells maintained similar connections with relay cells in the l.g.n. Cells in layers 3, 4, upper 5 and 6 were monosynaptically excited by geniculate afferents, while cells in layers 2 and lower 5 received only indirect excitation via other cortical neurons. Layer 3 cells were unique in receiving a prominent disynaptic e.p.s.p. in addition to the direct excitation from the l.g.n. Late, trisynaptic e.p.s.p. components were seen in many layer 5 and 6 cells. The orderly laminar arrangement of the connections had the consequence that identified cortico-geniculate neurons were monosynaptically excited and corticocollicular neurons di- and trisynaptically excited by geniculate afferents. Corticocortical neurons in layers 2 and 3 received di- or mono-plus disynaptic excitation, depending on laminar position. Post-synaptic inhibitory potentials were evoked in all impaled cells, following stimulation of the geniculo-cortical pathways. Except for a few layer 2 cells, this inhibition was mediated through disynaptic pathways of the feed-forward type. There was a good positive correlation between conduction times for monosynaptic e.p.s.p. and disynaptic i.p.s.p. in the same cells, suggesting that cortical neurons receive excitation and inhibition from the same type of geniculate afferents. The stimulating electrodes activated not only geniculo-cortical afferents, but antidromically activated cortical efferent neurons from their extracortical axons. These neurons possess intracortical collaterals, and care must be taken to distinguish the resulting potentials from those mediated by orthodromic activation of geniculate afferents. Evidence was obtained for excitatory connections from layers 2 and 3 to layer 5, from layer 5 to layer 6 and from layer 6 to layer 4. Typical recurrent inhibition was not observed. The receptive field properties of many neurons were examined before penetration. Simple cells were found in layers 4 and 6 and they all received prominent monosynaptic excitation from the l.g.n. Cells in layers 2, 3 and 5, as well as a few non-projecting cells in layer 6, had complex receptive fields. The connectivity of these cells varied with laminar position. Complex cells in layers 6 and upper 5 received direct excitation, those in 3 direct plus indirect excitation and those in 2 and lower 5 only indirect excitation from the l.g.n. The significance of these results for the construction of cortical receptive fields is discussed.