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Visual Efference Neuromodulates Retinal Timing: In Vivo Roles of Octopamine, Substance P, Circadian Phase, and Efferent Activation in Limulus

¹Sensory Coding Laboratory, Department of Psychological Sciences, Purdue University, West Lafayette; ²Department of Psychological and Brain Science, Indiana University, ³Department of Psychology, Monmouth College, Indiana, ⁴Division of Neuromuscular Disease, Department of Neurology, Harvard Medical School, and ⁵Department of Family Medicine, Akron General Medical Center, Ohio State University

Submitted 21 October 2008; accepted in final form 13 June 2009

Efferent nerves coursing from the brain to the lateral eye of the horseshoe crab, Limulus polyphemus, increase its nighttime sensitivity to light. They release octopamine, which produces a categorical increase of photoreceptor response duration in vitro. Analogous in vivo timing effects on the electroretinogram (ERG) were demonstrated when octopamine was infiltrated into the eye of an otherwise intact animal; nighttime ERGs were longer than daytime ERGs. Related effects on the ERG were produced by daytime electrical stimulation of efferent fibers. Surprisingly, in a departure from effects predicted solely from in vitro octopamine data, nighttime ERG onsets were also accelerated relative to daytime ERG onsets. Drawing on earlier reports, these remarkable accelerations led to an examination of substance P as another candidate neuromodulator. It demonstrated that infiltrations of either modulator into the lateral eyes of otherwise intact crabs increased the amplitude of ERG responses but that each candidate modulator induced daytime responses that specifically mimicked one of the two particular aspects of the timing differences between day- and nighttime ERGs: octopamine increased the duration of daytime ERGs and substance P infiltrated during the day accelerated response onset. These results indicate that, in addition to octopamine's known role as an efferent neuromodulator that increases nighttime ERG amplitudes, octopamine clearly also affects the timing of photoreceptor responses. But these infiltration data go further and strongly suggest that substance P may also be released into the lateral eye at night, thereby accelerating the ERG's onset in addition to increasing its amplitude.