Excitatory and differential disinhibitory actions of acetylcholine in the lateral geniculate nucleus of the cat

Abstract

Single neurones were recorded in the dorsal lateral geniculate nucleus (d.l.g.n.) of adult cats anaesthetized with a mixture of halothane, nitrous oxide and oxygen. The multibarrel-glass micro-electrodes were filled with sodium acetate, L-glutamate, acetylcholine (ACh), gamma-aminobutyric acid (GABA) and bicuculline. In normally innervated, spontaneously active d.l.g.n. cells, ACh and L-glutamate elicited increased firing rates. After elimination of the excitatory input from the retina by retinal photocoagulation, the effects of ACh and L-glutamate were similar. This proves that both drugs have direct excitatory effects on d.l.g.n. cells and that disinhibition is not the most prominent influence of ACh in the d.l.g.n. The excitatory action of ACh on relay cells in the d.l.g.n. was strongly influenced by barbiturates. Sub-narcotic levels of sodium pentobarbitone completely abolished the excitation by ACh while the response to L-glutamate remained unchanged. Excitation, centre-surround antagonism and periphery effects were elicited by spots of light and by large field phase-reversing gratings with and without central sparing of the receptive field area. Binocular inhibition was elicited with the phase-reversing grating presented to the non-dominant eye. After localized destruction of the retinal receptive field area, retinogeniculate excitation ceased and an isolated lateral inhibition was observed in the acutely deafferented d.l.g.n. cells. The time course and strength of this inhibition was disclosed by raising the background discharge with microiontophoretically applied L-glutamate. With increasing size of retinal lesions the strength of isolated lateral inhibition decreased exponentially. A maximal intrageniculate range of more than 1000 microns was derived from computations of the lateral extent of deafferentation in the d.l.g.n. The inhibition acted beyond the classic surround inhibition of d.l.g.n. cells and thus was named long-range lateral inhibition. Microiontophoretically applied GABA elicits a strong inhibitory effect at the d.l.g.n. cells which is antagonized by bicuculline. Centre-surround antagonism, binocular inhibition and long-range inhibition were blocked by bicuculline and thus proven to be GABAergic. Each class of inhibition was differentially influenced by microiontophoretically applied ACh. Long-range inhibition was disinhibited, centre-surround antagonism was enhanced, and binocular inhibition was not significantly changed. In contrast to ACh excitation, the disinhibitory action of ACh was not suppressed by pentobarbitone.(ABSTRACT TRUNCATED AT 400 WORDS)