Neuropeptide modulation of photosensitivity. I. Presence, distribution, and characterization of a substance P-like peptide in the lateral eye of Limulus

Abstract

The lateral eye of Limulus is innervated by an efferent system of fibers containing a substance P-like peptide. They were detected and their distribution was studied using indirect immunocytochemical techniques and monoclonal and serum antibodies. These thin, efferent fibers travel up the optic nerve, cross the lateral plexus, and branch out profusely when reaching the ommatidial layer. Innervation is extended to more than one component of the ommatidia, including the pigment, retinular, and eccentric cells. Immunoreactive staining could be abolished by absorbing the antisera with as little as 1 microM synthetic substance P. The efferent character of the fibers was established by means of ligation experiments, a technique also used to determine their origin in the circumesophageal connectives. Radioimmunoassay with two different C-terminal serum antibodies confirmed the presence of substance P-like material in the eye in the amounts of 61.44 pg/micrograms of protein, or up to 18 ng/eye. Gel filtration chromatography of crude extracts of the lateral eye, followed by radioimmunoassay, revealed an elution pattern extremely similar but not identical to that of synthetic substance P. These results show that a system of efferent fibers containing a substance P-like peptide originates in cells in the circumesophageal ring and innervates the ommatidia of the lateral eye. Their distribution and origin suggest an involvement in the modulation of photosensitivity, as part of a larger, generalized, level-setting regulator that is driven by a circadian clock but can also be activated by other systems.

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

“…Furthermore, as is described later in this review, application of octopamine to the eyes mimics many of the biochemical, electrophysiological, and anatomical effects of endogenous circadian efferent nerve activity (See Table 1). A second type of efferent projection to the lateral eyes has been described that consists of substance P (SP)-and FMRFamide-immunoreactive axons (Chamberlain and Engbretson, 1982;Mancillas and Brown, 1984;Mancillas and Selverston, 1985). But these SP/FMRFamide efferents are part of a general cuticular innervation and entirely separate from the octopaminergic system.…”

Immunocytochemical demonstration of locustatachykinin‐related peptides in the central complex of the locust brain

“…The antisubstance P antiserum (TG2-4), a gift from M.R. Brown (University of California, San Diego, CA), has been characterized by Mancillas and Brown (1984). Its specificity in locust brain tissue has been shown by Wü rden and .…”

A circadian clock in the Limulus brain transmits synchronous efferent signals to all eyes

“…4 showed that partial bisection of the brain desynchronized the burst activity from efferent fibers from the two halves of the brain. Mancillas and Brown (1984) concluded that efferent fibers from the circadian clock exit the brain from dorsal nerves 3 and 4 and terminate in the lateral eye. Anatomical studies show that the efferent cell bodies are located in the chelicera ganglion (Caiman & Battelle, 1991;Lee & Wyse, 1991) and send nerve fibers out ipsilateral optic nerve trunks as well as across the midline to the contralateral side.…”