Categorical and Prolonged Potentials Are Evoked when Brief, Intermediate-Intensity Flashes Stimulate Horseshoe Crab Lateral Eye Photoreceptors during Octopamine Neuromodulation

Abstract

Octopamine, a major efferent neurotransmitter in the lateral eye of the horseshoe crab (Limulus polyphemus), has previously been shown to modulate photoreceptor responses evoked by long flashes. Quantification of these data indicates that this modulation produced a genuine increase in sensitivity to light which cannot be entirely due to an increase in optical efficiency consequent on an anatomical alteration. Other previous studies demonstrated that extrinsic current can modulate Limulus lateral eye photoreceptor cells by inducing a bistable membrane potential with two distinct states. The present study was therefore undertaken to find out if octopamine could modulate visual responses by inducing prolonged and bistable polarization shifts similar to those demonstrated in several other neural systems. Intracellular microelectrodes were used to execute an electrophysiological study of the receptor potentials evoked in the lateral eye of Limulus when brief (20-ms) flashes were delivered while 50 µM octopamine perfused dark-adapted photoreceptors. The combined chemical and optical stimuli prolonged photoreceptor responses to light to the degree that they often exceeded the duration of the brief stimulus by hundreds of milliseconds. Moreover, these prolonged potentials were clearly bistable because they were categorical – either a prolongation was perceptually clear-cut and present or it was not, with no intermediate patterns being observed. During seawater control perfusions, such prolongations were absent. This appears to be the first demonstration of such categorical and prolonged potentials in a photoreceptor neuron. This finding particularly suggests that efferent-driven neuromodulation can enable the development of a persisting short-term representation of a brief stimulus, with this representation being retained at the most distal possible neural site.

Stable bellows cup electrode demonstrates low-frequency properties of long-term electroretinographic recordings in the Limulus lateral eye

“…This procedure demonstrated dramatic effects of octopamine on the temporal properties of receptor potentials in vitro. We particularly found (Lim and Wasserman, 2001) that octopamine radically prolonged receptor responses, an effect that had not been observed by others who had used very long steps of light which produced stimulus-bound responses which were prolonged ipso facto. This raised the question of whether comparable timing changes occurred in intact animals.…”

Hygienic behavior in the honey bee (Apis mellifera L.) and the modulatory role of octopamine

“…In a number of invertebrate preparations, it has been well documented that OA can modulate the sensitivity of various types of sensory systems (Ramirez and Orchard, 1990;Zhang et al, 1992;Pophof, 2000Pophof, , 2002Dolzer et al, 2001;Grosmaitre et al, 2001;Lim and Wasserman, 2001). For example, OA has been shown to modulate neuronal firing activity and to increase the amplitude of receptor potentials in the pheromone-sensitive antennal neurons of the male moth, Bombyx mori, but not the receptor potentials of olfactory neurons in other moth species (Pophof, 2000;Grosmaitre et al, 2001).…”

A Top–Down and Bottom–Up Component of Visual Attention

“…We quickly observed [24] that such was the case for efference in Limulus. Our first discovery came when we simply used our existing laboratory procedures to replicate the circadian findings of others who had studied this crab.…”