Circadian efferent input to Limulus eyes: Anatomy, circuitry, and impact

Abstract

Much is known about the anatomy of Limulus retinal efferent neurons and the structural and functional consequences of their activation. Retinal efferent axons arise from cell bodies located in the cheliceral ganglia of the brain, and they project out all of the optic nerves. Their unique neurosecretory-like terminals contact all cell types in lateral eye ommatidia, the retinular cells of the median eye, and the internal rhabdom of ventral photoreceptors. Lateral and median rudimentary photoreceptors are also innervated. The activity of the efferents is circadian. They are active during the subjective night and inactive during the subjective day. Activation of the efferents drives dramatic and diverse changes in the structure and function of Limulus eyes and causes the sensitivity and responsiveness of the eyes to light to increase at night. Relatively little is known about the molecular mechanisms that produce these structural and functional changes, but one efferent-activated biochemical cascade has been identified. The biogenic amine octopamine is released from efferent terminals, and an octopamine-stimulated rise in cAMP in photoreceptors, with a subsequent activation of cAMP-dependent protein kinase, mediates many of the known effects of efferent input. A photoreceptor-specific protein, myosin III, is phosphorylated in response to efferent input; this protein may play a role in the efferent stimulated changes in photoreceptor structure and function. Anatomical, biophysical, biochemical, and molecular approaches are now being effectively combined in studies of Limulus eyes; thus, this preparation should be particularly useful for further detailed investigations of mechanisms underlying the modulation of primary sensory cells by efferent input.

Opsin1-2, Gqα and arrestin levels at Limulus rhabdoms are controlled by diurnal light and a circadian clock

“…Many effects of the clock are mimicked by OA and by elevating cAMP in photoreceptors (Battelle, 2002;Dalal and Battelle, 2010). Therefore, we tested in vitro whether OA, which activates adenylyl cyclase-coupled receptors, or forskolin, a direct activator of adenylyl cyclase, mimic the effects of clock input on RhOps1-2, RhOps5, RhG q α or RhArr levels during daytime dark adaptation.…”

“…OA stimulates a rise in cAMP in Limulus photoreceptors (Kaupp et al, 1982) and LE slices (Dalal and Battelle, 2010), and many of the known effects of clock input to LEs are mimicked by OA and other treatments that activate the cAMP cascade (reviewed in Battelle, 2002;Dalal and Battelle, 2010).…”

Evolution of arthropod visual systems: Development of the eyes and central visual pathways in the horseshoe crabLimulus polyphemusLinnaeus, 1758 (Chelicerata, Xiphosura)

“…Aspects that have been explored in the past include adult ommatidial morphology of the lateral eyes (review Fahrenbach, 1975), organization of the retinal projections into the brain as well as efferent projections Barlow, 1980, 1982;Batra and Chamberlain, 1985;, and distribution of the visual pathway neurotransmitters (reviewed in Battelle et al, 1999) octopamine (Evans et al, 1983), serotonin , FMRFamide and substance P (Chamberlain and Engbretson, 1982;Lewandoswski et al, 1989), histamine , and acetylcholine (Hornstein et al, 1994). Additionally, circadian modulation of the photoresponse (e.g., Battelle et al, 1998Battelle et al, , 2000Battelle et al, , 2001Sacunas et al, 2002;Waren and Chamberlain, 2002;Ankrom and Chamberlain, 2002;Dalal et al, 2003;Pieprzyk et al, 2003;Runyon et al, 2004;reviews, Barlow, 2001;Battelle, 2002), and both computational and behavioral aspects of vision (reviewed in Barlow et al, 2001) are active areas of current research.…”

Chemical cues from fish heighten visual sensitivity in larval crabs through changes in photoreceptor structure and function

“…Specific neural inputs that mediate sensitivity changes are rarely reported. However, intracellular electrophysiological recordings in Limulus suggest that efferent input from the optic nerve plays an important role in increasing response gain in photoreceptor cells and that octopamine probably acts as the neurotransmitter for these optic nerve pulses Battelle, 2002;Kaplan and Barlow, 1980). Alternatively, Blest and Stowe (1997) found that inhibition of phospholipase, an enzyme that is important for phototransduction, prevented the diurnal decreases in rhabdom diameter that occur during the diel cycle of an adult crab.…”

“…In a vertical migration scenario, for instance, this might place zooplankton at overall deeper depths in the water column throughout the diel cycle (Forward, 1985). Visual sensitivity may be controlled by structural and/or physiological mechanisms, as both play important roles mediating diel changes in visual sensitivity in crustaceans (Meyer-Rochow, 1999) and other arthropods (Battelle, 2002;Warrant et al, 2014). Here, electroretinogram (ERG) recordings and histological methods are employed to investigate kairomone-induced changes to retinal physiology and eye structure that could increase visual sensitivity and thereby result in kairomone-induced increases in photobehavior.…”