Circadian rhythmicity in Bulla gouldiana: Role of the eyes in controlling locomotor behavior

Abstract

The eyes of B u l k express a circadian rhythm in optic nerve impulse frequency. Bulla also exhibit a circadian rhythm in locomotor behavior. In order to determine what role the ocular oscillators play in controlling rhythmic behavior, the eyes were removed and locomotor activity was recorded during free runs and while entrained to light-dark cycles. We find that eye removal leads to a disorganization of the free-running locomotor rhythm, suggesting that the ocular oscillators are involved in timing this behavior. Eyeless Bulla in the presence of light cycles exhibit locomotor rhythmicity but there is a switch from predominantly nocturnal to diurnal activity. While diurnal behavior in eyeless Bulla reveals the presence of extraocular photoreceptors, we presently find no evidence that a circadian pacemaker mediates this diurnal activity.

The influence of light on locomotion in the gastropodmelibe leonina

“…Many other gastropods are known to have an endogenous activity rhythm, including Aplysia californica (Jacklet, 1969;Lickey et al, 1977), Arion ater (Lewis, 1969), Bulla gouldiana (Block and Davenport, 1982), Bursatella leachi (Block and Roberts, 1981), Helisoma trivolvis (Kavaliers, 1981), Limax maximus (Beiswanger et al, 1981), and Melanoides tuberculata (Beeston and Morgan, 1979), though, of these species, only B. gouldiana, H. trivolvis and L. maximus are nocturnal. The continued activity rhythm seen in constant darkness with M. leonina disappeared in constant light.…”

“…The influence of light on the locomotor activity of gastropods has been investigated in a number of species including Aplysia californica (Kupfermann, 1968;Kupfermann and Carew, 1974), Arion ater (Lewis, 1969), Bulla gouldiana (Block and Davenport, 1982), Bursatella leachi (Block and Roberts, 1981;Ramos et al, 1995), Helisoma trivolvis (Kavaliers, 1981), Limax maximus (Sokolove et al, 1977), and Melanoides tuberculata (Beeston and Morgan, 1979). These animals display three different patterns of activity: some are nocturnal (B. gouldiana, H. trivolvis, and L. maximus), some diurnal (A. californica, A. ater, B. leachi), and one is even distinctly crepuscular (M. tuberculata).…”

Sequences of Circadian Clock Proteins in the Nudibranch Molluscs Hermissenda crassicornis, Melibe leonina, and Tritonia diomedea

“…Subsequently, circadian rhythms of locomotion, oxygen consumption, and ocular electrical activity have been identified in several other gastropods, including Bulina tropicas (Chaudhry and Morgan, 1983), Bulla gouldiana (Block and Davenport, 1982), Bursatella leachi (Block and Roberts, 1981), Helisoma trivolvis (Kavaliers, 1981), Helix aspersa (Bailey, 1981; Blanc, 1993), Hydrobia ulvae (Barnes, 1986), Limax maximus (Sokolove et al, 1977), Littorina irrorata (Shirley and Findley, 1978), Melanerita atramentosa (Zann, 1973), Melanoides tuberculata (Beeston and Morgan, 1979), and Melibe leonina (Newcomb et al, 2014). However, despite strong interest in gastropod circadian rhythms, and the advantages of this group of animals for investigating the neuronal bases of behaviors, there has been very little progress in identifying circadian genes in gastropods, with the exception of the transcript for period in Bulla gouldiana (Constance et al, 2002), the basic helix-loop-helix (bHLH)-containing proteins BMAL1 and CLOCK in Biomphalaria glabrata, Lottia gigantea , and Patella vulgate (Bao et al, 2017), and some automated annotations on GenBank at the National Center for Biotechnology Information (NCBI, Bethesda, MD).…”

The circadian rhythm and photosensitivity of small impulses of the Bulla eye

“…Finally, the circadian rhythm in the frequency of small-spikes from the eye could be providing the rest of the animal with temporal information involved in locomotion. Bulla become arrhythmic in DD after eye removal (Block and Davenport 1982), but this experiment does not discriminate between information carried in the frequency of CAPs or small-spikes.…”

“…The rhythm appears to govern locomotor activity, since Bulla in constant darkness (DD) become arrhythmic following eye removal (Block and Davenport 1982). Also, the circadian Abbreviations: A S W artificial sea water; BRN basal retinal neuron; CAP compound action potential rhythm in CAPs from each eye functions to keep the pacemaker in phase with the pacemaker of the contralateral eye (Roberts and Block 1983).…”