Circadian and ultradian rhythms in the crayfish caudal photoreceptor

Abstract

The study of circadian clocks in crustaceans has led to the hypothesis of a distributed circadian system of pacemakers. In this review, we investigate the role of the crayfish caudal photoreceptor (CPR) as a candidate to form part of this pacemaking circadian system. Two circadian rhythms are documented for CPR electrical activity. These rhythms correspond to the spontaneous and light-induced discharge of action potentials. The intrinsic characterization of the rhythms is made through the analysis of the firing rate of the corresponding action potentials. The discharges were extracellularly recorded in the isolated 6th abdominal ganglion (AG) in an organ culture kept at constant temperature for up to 5 days. For preparations kept in the dark, spontaneous activity varies in a circadian manner, with a period of 24.7 h and the acrophase at subjective nighttime (2140). For light-induced activity, pulses of constant intensity applied regularly throughout the 24-h cycle show that the firing rate at peak and latency vary rhythmically. The period for this rhythm is 24.24 h and the acrophase is at subjective dawn (0326). Additionally, an ultradian rhythm of a approximately 12-h period was observed for both rhythms. When tested with light pulses of different intensities, the CPR responsiveness at night is almost one log unit greater than in daytime. The effect of temperature on both activities is also described. The phase-shift caused by temperature for these circadian rhythms depends on the application time. These results show that the 6th AG is capable of generating a circadian rhythm of electrical activity in the CPR, which in turn is likely to be part of the crayfish circadian system. A possible interaction of different pacemakers forming the distributed circadian system is also discussed. The role of serotonin as a possible modulator of the CPR electrical activity is documented. In addition, the level of the 5-HT(1A) receptors displays a diurnal rhythm in the 6th AG, with the acrophase at twilight (1849). We suggest that the 5-HT(1A) receptor does participate in this modulation. Finally, the hypothesis of the expression of two circadian oscillators in a single identified neuron is presented.

Circadian clocks in crustaceans: identified neuronal and cellular systems

“…This has been interpreted as a result of circadian changes in the sensitivity of the CPR. Thus, the CPR shows circadian rhythms in activity as well as in sensitivity, the latter being comparable to the intrinsic rhythmicity characteristic for the retinal ERG (12). It is intriguing that both the light sensitivity and the circadian activity reside in the same oscillator neuron.…”

“…Whilst ultradian rhythms have been detected in many systems (12), their functional significance has yet to be determined. They are often excluded from further analyses (23), which may well leave aspects of great biological importance unrecognised.…”

“…Thus, the CPR has subtle regulatory functions, which may depend upon the length and intensity of light input. Extracellular electrophysiological recordings have recently shown that the crayfish CPR itself displays circadian rhythms of spontaneous as well as regularly light-induced action potential discharges with only slightly differing periods (24.7hr vs. 24.25hr) but very different acrophases at night time (21:40hr) or dawn (03:26hr), respectively, in isolated ganglia (12). In addition, ultradian components of ca.…”

Chronic electromyographic analysis of circadian locomotor activity in crayfish

“…We demonstrated by chronic EMG recording that the locomotor behavior was initiated spontaneously, not reflexively by any external stimulus. It has been proposed that the locomotory circadian rhythmicity of P. clarkii is generated by clock proteins and regulated by hormonal and neuromodulator secretion in the brain [3,41,43] and also is regulated by photoreceptors in the brain [37,38,43] or in the 6 th abdominal ganglion [56,57]. Although the details of interaction cascades among those factors remain unknown, the brain should play an important role for the circadian locomotor activity [3,38,43].…”

“…Previous studies using Procambarus bouvieri showed that there was a correlation between the rhythms of ERG and locomotor activity in intact and brainless crayfish [27], and that its caudal photoreceptors functioned as a circadian photoreceptor [55]. Recent research using Procambarus clarkii and Cherax quadricarinatus suggests that the caudal photoreceptor contributes to the entrainment of circadian locomotor activity [56,57]. Meanwhile, other studies using P. clarkii demonstrated that the brain photoreceptors are necessary for the entrainment of locomotor activity rhythms to light stimuli [38], and that they can function in the absence of the compound eyes and caudal photoreceptors [37,43].…”