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

Abstract

SUMMARY1. The latencies ofexcitatory and inhibitory post-synaptic potentials (e.p.s.p.s and i.p.s.p.s) evoked by electrical stimulation of afferents from the lateral geniculate nucleus were recorded in neurones ofarea 17 of the cat visual cortex. After application of an extrapolation procedure to compensate for the conduction time of the afferent axons, a histogram oflatencies formed three distinct peaks. Potentials in each ofthese were interpreted as being mediated by mono-, di-and trisynaptic pathways.2. Characteristic laminar differences in the extracellular field potentials evoked from the lateral geniculate nucleus (l.g.n.) and in the antidromic activation of neurones from the l.g.n. and superior colliculus were used to determine the laminar position of recorded neurones. It was found that within a given layer, all cells maintained similar connexions 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 neurones. 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.3. The orderly laminar arrangement of the connexions had the consequence that identified cortico-geniculate neurones were monosynaptically excited and corticocollicular neurones di-and trisynaptically excited by geniculate afferents. Corticocortical neurones in layers 2 and 3 received di-or mono-plus disynaptic excitation, depending on laminar position.4. Post-synaptic inhibitory potentials were evoked in all impaled cells, following stimulation of the geniculo-cortical pathway. Except for a few layer 2 cells, this inhibition was mediated through disynaptic pathways ofthe feed-forward type. There was a good positive correlation between conduction times for monosynaptic e.p.s.p.s and disynaptic i.p.s.p.s in the same cells, suggesting that cortical neurones receive excitation and inhibition from the same type of geniculate afferents.5. The stimulating electrodes activated not only geniculo-cortical afferents, but antidromically activated cortical efferent neurones from their extracortical axons. These neurones possess intracortical collaterals, and care must be taken to distinguish

Short-Term Depression in Thalamocortical Synapses of Cat Primary Visual Cortex

“…Synaptic potentials arising from these two distinct pathways differ in latency (Ferster and Lindström, 1983), with disynaptic inputs arriving at least 1 ms later than monosynaptic inputs (and trisynaptic inputs arriving at least 2 ms later). Many cortical cells receive both monosynaptic and polysynaptic excitatory inputs.…”

“…3B). The division between putative monosynaptic and polysynaptic cells was chosen based on the shape of the distribution of measured latencies, as well as on previous studies using similar methods (Ferster and Lindström, 1983;Chung and Ferster, 1998).…”

Diverse Types of Interneurons Generate Thalamus-Evoked Feedforward Inhibition in the Mouse Barrel Cortex

“…Interestingly, this is also the main direction of flow of excitation mediated by spiny stellate and star pyramidal cells' axons (Lund et al, 1979;Ferster and Lindstrom, 1983;Armstrong-James et al, 1992;Anderson et al, 1994;Lubke et al, 2000). Thus, inhibition in the cortex is inextricably linked to excitation, apparently following it along its intracortical course.…”

“…Because putative inhibitory barrel neurons often have multiwhisker receptive fields (Simons and Carvell, 1989;Swadlow, 1989;Welker et al, 1993), type A neurons may also mediate the adjacent-whisker inhibition observed in vivo (Simons, 1995;Goldreich et al, 1999). Types B, D, and E neurons, with a sphere of influence extending to layers II/III, probably mediate the strong disynaptic inhibition observed in supragranular neurons in vivo (Ferster and Lindstrom, 1983;Kyriazi et al, 1998;Brumberg et al, 1999;Zhu and Connors, 1999) or in vitro (Agmon and Connors, 1992). Finally, inhibitory neurons of morphological type E, with axonal trees that extend tangentially at least one barrel width on either or both sides of the column of origin, will generate the short-latency cross-column inhibition that is a prominent feature in supragranular layers of mouse barrel cortex in vivo (Welker et al, 1993).…”

“…Although the thalamocortical input to the neocortex is purely excitatory (glutamatergic), as determined by electrophysiological, electron microscopic, and immunocytochemical evidence (White, 1978;Ferster and Lindstrom, 1983;Agmon and Connors, 1992;Kharazia and Weinberg, 1993), inhibitory (GABAergic) mechanisms are recruited from the very first stage of intracortical processing. Indeed, electrical stimulation of thalamocortical afferents in vivo (Ferster and Lindstrom, 1983;Swadlow, 1989Swadlow, , 1990 or in vitro (Agmon and Connors, 1992;Gil and Amitai, 1996), as well as controlled sensory stimulation (Simons and Carvell, 1989;Simons, 1995;Brumberg et al, 1996;Swadlow et al, 1998;Zhu and Connors, 1999), result in a brief excitation of neocortical neurons, immediately followed by a pronounced inhibitory response mediated by intracortical inhibitory interneurons. The short latency of the inhibitory response indicates that the inhibitory interneurons eliciting it must be excited directly by the thalamocortical afferents, consistent with anatomical data (White, 1978;Fairén and Valverde, 1979;Freund et al, 1985;Keller and White, 1987), and in turn inhibit other cortical neurons disynaptically.…”