Cholinergic synapses and the organization of contrast detection in the crayfish optic lobe

The actions of acetylcholine (ACh) were examined on 4 classes of multicolumnar interneurons whose dendrites lie in close proximity to the putative cholinergic transmedullary neurons described in the companion report. ACh-elicited responses in each cell type resemble visually elicited synaptic events and persist following synaptic blockade with 20 mM CoCl2. Tangential cells exhibit a hyperpolarizing response to ACh that resembles the visual response in reversal potential and dependence on extracellular chloride. The visual response is potentiated by the anticholinesterase, neostigmine (0.1 mM). Visual and carbachol-elicited responses are blocked by nicotinic ganglionic antagonists (e.g., 10(-6) M pempidine) that are 10-100 times more potent than D-tubocurarine. Medullary amacrine cells exhibit depolarizing responses to ACh (10(-6) M) and light with similar reversal potentials. The visual response is potentiated by neostigmine. Dimming fibers respond to light and ACh with a hyperpolarization that inhibits the maintained discharge. The sustaining fiber response to ACh reflects both direct responses and indirectly elicited synaptic actions. The direct action is a hyperpolarization possibly related to the visual "off-response." It is associated with an increased conductance and a reversal potential negative to the dark potential. The off-response is abolished by curare and pempidine and potentiated by neostigmine. ACh appears to orchestrate several aspects of the dual-channel contrast detection system of the optic lobe. The actions of ACh on tangential cells, amacrine cells, and dimming fibers are all consistent with the effects of a spatially localized increment in light intensity and a corresponding local release of ACh in the retinotopic columnar array.