Light and drug effects reveal three pathways for nitric oxide modulation of the first visual synaptic relay in the lamina ganglionaris.

Abstract

The modulation of synaptic relay mechanisms in the visual pathway remains a significant area of investigation. Here, we explore the role of nitric oxide (NO) in the eyestalks of the Australian blue crayfish Cherax quadricarinatus, focusing on its relationship with light exposure and potential regulatory pathways involving NO promoters and inhibitors. NO levels in the eyestalks were assessed using the Griess technique under various light-dark cycles and different physiological parameters (size, weight and sex) of adult crayfish. We found a light-dependent modulation of NO concentration, with constant light exposure significantly elevating NO levels compared with periods where darkness is involved and a negative trend as darkness increased. Interestingly, size, weight and sex variations showed no discernible impact on NO levels. Moreover, the influence of histamine (a primary neurotransmitter involved in the first visual synaptic relay) and a nitric oxide synthase (NOS) inhibitor, such as NG-nitro-l-arginine methyl ester (l-NAME), or the H2-blocker ranitidine, was investigated. As expected, histamine notably enhanced NO synthesis, whereas NOS inhibitors and H2 blockers led to substantial reductions in nitrite concentrations. The findings point to three possible mechanisms of action: (i) a light-induced release of histamine from retinal photoreceptors that activates postsynaptic receptors in lamina ganglionaris monopolar neurons, inducing NO synthesis and retrograde modulation of the photoreceptor; (ii) a histamine-dependent activation of postsynaptic receptors in monopolar cells that promotes NOS-mediated NO production, which retrogradely recruits lamina interneurons (e.g. GABAergic horizontal/amacrine cells) to mediate lateral inhibition of photoreceptors through GABA and/or ACh; and (iii) a mechanism in which light-induced histamine release activates photoreceptor auto-receptors, leading to NO release from the photoreceptor to cells of the lamina ganglionaris.