The functional influence of nicotinic cholinergic receptors on the visual responses of neurones in the superficial superior colliculus

In the rat, the superficial gray layer (SGS) of the superior colliculus rec eives glutamatergic projections from the contralateral retina and from the visual cortex. A few fibers from the ipsilateral retina also directly inner vate the SGS, but most of the ipsilateral visual input is provided by choli nergic afferents from the opposing parabigeminal nucleus (PBG). Thus, visua l input carried by cholinergic afferents may have a functional influence on the responses of SGS neurones. When single neuronal extracellular recordin g and iontophoretic drug application were employed to examine this possibil ity, cholinergic agonists were found to depress responses to visual stimula tion. Lobeline and 1-acetyl-4-methylpiperazine both depressed visually evok ed activity and had a tendency to reduce the background firing rate of the neurones. Carbachol depressed the visual responses without any significant effect on the ongoing activity, while the muscarinic receptor selective ago nist methacholine increased the background activity of the neurones and red uced their visual responses. Lobeline was chosen for further studies on the role of nicotinic receptors in SGS. Given that nicotinic receptors are ass ociated with retinal terminals in SGS, and that the activation of presynapt ic nicotinic receptors normally facilitates transmitter release (in this ca se glutamate release), the depressant effects of nicotinic agonists are int riguing. However, many retinal afferents contact inhibitory neurones in SGS ; thus it is possible that the increase in glutamate release in turn facili tates the liberation of GABA which goes on to inhibit the visual responses. We therefore attempted to reverse the effects of lobeline with GABA recept or antagonists. The depressant effects of lobeline on the visual response c ould not be reversed by the GABA(A) antagonist bicuculline, but the GABA(B) antagonist CGP 35348 reduced the effects of lobeline. We hypothesize that cholinergic drive from the parabigeminal nucleus may activate presynaptic n icotinic receptors on retinal terminals, thereby facilitating the release o f glutamate onto inhibitory neurones. Consequently GABA is released, activa ting GABA(B) receptors, and thus the ultimate effect of nicotinic receptor activation is to depress visual responses.