Brain Photoreceptor Pathways Contributing to Circadian Rhythmicity in Crayfish

Abstract

Freshwater crayfish have three known photoreceptive systems: the compound eyes, extraretinal brain photoreceptors, and caudal photoreceptors. The primary goal of the work described here was to explore the contribution of the brain photoreceptors to circadian locomotory activity and define some of the underlying neural pathways. Immunocytochemical studies of the brain photoreceptors in the parastacid (southern hemisphere) crayfish Cherax destructor reveal their expression of the blue light-sensitive photopigment cryptochrome and the neurotransmitter histamine. The brain photo-receptors project to two small protocerebral neuropils, the brain photoreceptor neuropils (BPNs), where they terminate among fibers expressing the neuropeptide pigment-dispersing hormone (PDH), a signaling molecule in arthropod circadian systems. Comparable pathways are also described in the astacid (northern hemisphere) crayfish Procambarus clarkii. Despite exhibiting markedly different diurnal locomotor activity rhythms, removal of the compound eyes and caudal photoreceptors in both C. destructor and P. clarkii (leaving the brain photoreceptors intact) does not abolish the normal light/dark activity cycle in either species, nor prevent the entrainment of their activity cycles to phase shifts of the light/dark period. These results suggest, therefore, that crayfish brain photoreceptors are sufficient for the entrainment of loco-motor activity rhythms to photic stimuli, and that they can act in the absence of the compound eyes and caudal photoreceptors. We also demonstrate that the intensity of PDH expression in the BPNs varies in phase with the locomotor activity rhythm of both crayfish species. Together, these findings suggest that the brain photoreceptor cells can function as extraretinal circadian photoreceptors and that the BPN represents part of an entrainment pathway synchronizing locomotor activity to environmental light/dark cycles, and implicating the neuropeptide PDH in these functions. (Author correspondence: bbeltz@wellesley.edu)

An ancient cytokine, astakine, mediates circadian regulation of invertebrate hematopoiesis

“…Astacid crayfish are known to have their main locomotion activity restrained to the dark period, and usually their activity increases immediately when the light turns off, and then an activity peak is often found immediately before dawn [21,23]. The expression of astakine 1 mRNA follows a similar pattern with very low expression before the light turns off, and then a rapid increase followed by a slightly lower expression during the night and then peak levels at dawn (Fig.…”

“…Photoperiodic rhythmicity has been shown to influence several processes in freshwater crayfish and these animals have served as models for studies in circadian locomotion activity [21][22][23]. Astacid crayfish are known to have their main locomotion activity restrained to the dark period, and usually their activity increases immediately when the light turns off, and then an activity peak is often found immediately before dawn [21,23].…”

Crustacean neuropeptides

“…In fact, in the STNS, where immunoreactivity is present, b-PDH shows no bioactivity [194]. Anecdotal evidence suggests that the PDH system in crustaceans may also be involved in the generation of circadian rhythmicity [196][197][198].…”

Neuroanatomy of the optic ganglia and central brain of the water flea Daphnia magna (Crustacea, Cladocera)

“…We were not able to reproducibly show HIS-ir in the D. magna Nauplius eye photoreceptors and the NEN, whereas this is known for similar photoreceptors from branchiopod and barnacle species (Callaway and Stuart 1989;Harzsch and Glötzner 2002) and for comparable extra-retinal brain photoreceptor neurons (BPNs) in the crayfish Cherax destructor (Sullivan et al 2009). Within the PB of this crayfish, HIS-ir BPNs connect to PDH-ir neurons, which are thought to confer light-dependent circadian locomotor rhythmicity (Sullivan et al 2009). In D. magna, we found neither HIS-ir nor PDH-ir in the PB, which consists of bilaterally symmetrical bipartite subdomains, a feature typical of other branchiopod PBs (Harzsch and Glötzner 2002).…”

“…In most other cladocerans, this neuropile has received little attention Harzsch and Glötzner 2002). We were not able to reproducibly show HIS-ir in the D. magna Nauplius eye photoreceptors and the NEN, whereas this is known for similar photoreceptors from branchiopod and barnacle species (Callaway and Stuart 1989;Harzsch and Glötzner 2002) and for comparable extra-retinal brain photoreceptor neurons (BPNs) in the crayfish Cherax destructor (Sullivan et al 2009). Within the PB of this crayfish, HIS-ir BPNs connect to PDH-ir neurons, which are thought to confer light-dependent circadian locomotor rhythmicity (Sullivan et al 2009).…”