Understanding the intrinsic circuitry of the cat’s lateral geniculate nucleus: electrical properties of the spine-triad arrangement

Abstract

Electron-microscopic studies of relay cells in the lateral geniculate nucleus of the cat have shown that the retinal input to X-cells is associated with a special synaptic circuitry, termed the spine-triad. The retinal afferent makes an asymmetrical synapse with both a dendritic appendage of the X-cell and a geniculate interneuron. The interneuron contacts in turn the same dendritic appendage with a symmetrical synaptic profile. The retinal input to geniculate Y-cells is predominantly found on dendritic shafts without any triadic arrangement. We explore the integrative properties of X- and Y-cells resulting from this striking dichotomy in synaptic architecture. The basis of our analysis is the solution of the passive cable equation in a HRP-stained and reconstructed geniculate X-cell with known somatic input resistance. Recent evidence shows that geniculate interneurons stain for glutamic acid decarboxylase, the synthesizing enzyme for the inhibitory neuro-transmitter γ- aminobutyric acid (GABA). Under the assumption that the GABAergic inhibition has a reversal potential close to the resting potential of the cell, activation of the interneuron reduces very efficiently the excitatory postsynaptic potential induced by the retinal afferent without affecting the electrical activity in the rest of the cell. Therefore, the spine—triad circuit implements the analogue version of an AND—NOT gate. Functionally, this corresponds to a presynaptic, feed-forward type of inhibition of the optic tract terminal although inhibition actually occurs at a postsynaptic site. If the inhibition has a reversal potential well below the resting potential, the inhibitory postsynaptic potential would hyperpolarize large parts of the relay cell, abolishing the local character of the synaptic veto operation. Since Y-cells lack this structure, inhibition acts globally, reducing the general electrical activity of the cell. We propose that geniculate interneurons gate the flow of visual information into the X-system as a function of the behavioural state of the animal, enhancing the centre-surround antagonism and possibly mediating reciprocal lateral inhibition and eye-movement-related suppression.