Properties of histamine-activated chloride channels in the large monopolar cells of the dipteran compound eye: a comparative study

Abstract

The large monopolar cells (LMCs) of the first optic neuropil (lamina) in insects respond to the photoreceptor neurotransmitter histamine with an increase in chloride conductance. We have compared the properties of this conductance from a range of diptera from different visual environments: Tipula paludosa (slow flying, crepuscular), Drosophila melanogaster (slow-flying diurnal), and 3 fast-flying diurnal species Musca domestica, Calliphora vicina and Lucilia sericata. In whole-cell recordings of dissociated LMCs, histamine-induced currents were elicited using a multichannel parallel perfusion device, allowing rapid determination of the dose-response function, characterised by affinity (Kd) and Hill coefficient (n). Calliphora, Lucilia and Musca had the steepest dose response curves (n = 2.8) and the lowest affinity for histamine (Kd 35–50 μM); the crepuscular Tipula had a significantly higher affinity (Kd = 16 μM) and lower Hill coefficient (n = 1.8). Drosophila had a high affinity (Kd 24 μM), and a high Hill coefficient (n = 2.5). In excised inside-out patch recordings all species showed similar single channel properties (conductance 40–60 pS, mean open time < 1 ms). The low Hill coefficient in Tipula would be expected to result in lower synaptic gain. We suggest this may be an adaptation to prevent the LMC's response bandwidth being filled with the high levels of photon noise typical of photoreceptors adapted for low light levels. The lower affinity for histamine found in the more photopic species suggests that the concentration of histamine (and therefore presumably number of synaptic vesicles released from the photoreceptors) should be higher. This might improve signal-to-noise ratio by decreasing the contribution of the shot event noise introduced by stochastic release of synaptic vesicles.