Circadian Regulation of Olfactory Receptor Neurons in the Cockroach Antenna

Abstract

In the cockroach, olfactory sensitivity as measured by the amplitude of the electroantennogram (EAG) is regulated by the circadian system. We wished to determine how this rhythm in antennal response was reflected in the activity of individual olfactory receptor neurons. The amplitude of the electroantennogram (EAG) and the activity of olfactory receptor neurons (ORNs) in single olfactory sensilla were recorded simultaneously for 3–5 days in constant darkness from an antenna of the cockroach Leucophaea maderae. Both EAG amplitude and the spike frequency of the ORNs exhibited circadian rhythms with peak amplitude/activity occurring in the subjective day. The phases of the rhythms were dependent on the phase of the prior light cycle and thus were entrainable by light. Ablation of the optic lobes abolished the rhythm in EAG amplitude as has been previously reported. In contrast, the rhythm in ORN response persisted following surgery. These results indicated that a circadian clock outside the optic lobes can regulate the responses of olfactory receptor neurons and further that this modulation of the ORN response is not dependent on the circadian rhythm in EAG amplitude.

Daily rhythms in antennal protein and olfactory sensitivity in the malaria mosquito Anopheles gambiae

“…This indicates that reduced sensitivity at ZT8 is not an acute effect of light on the function of the antennae, but in fact a reflection of an underlying circadian clock and/or diel regulated mechanism (driven by the environmental 24 hr LD cycle)8. Further, 24 hr rhythmic changes in electrophysiological sensitivity persist in constant dark (DD) conditions in Drosophila and cockroaches2123, and are driven by peripheral clocks located in the Drosophila antennae themselves39. Therefore, it is likely that the observed time-of-day changes in EAG sensitivity in An.…”

“…Tsetse flies, Drosophila and cockroaches have rhythmic daily changes in olfactory sensitivity212223, and An. gambiae exhibit diel and circadian rhythms of Blood-feeding behavior15.…”

Perfusion with cAMP analogue affects pheromone-sensitive trichoid sensilla of the hawkmothManduca sextain a time-dependent manner

“…In addition, our results suggest that circadian changes in odour sensitivity in moths are also regulated at the periphery as they are in D. melanogaster (Tanoue et al, 2004;Krishnan et al, 2008), cockroaches (Saifullah and Page, 2009) and other moths (Merlin et al, 2007). The endogenous decline in the mean SP amplitude, AP frequency, and the spontaneous AP activity during the photophase suggests that the observed circadian rhythms in pheromone sensitivity are at least partly due to time-dependent regulation of single ORNs.…”

A comparative view of insect circadian clock systems

“…Although circadian EAG rhythms have also been reported for cockroaches [120] and moths [121,122], the regulatory mechanism differs substantially from that of Drosophila described above. The EAG rhythms in cockroaches are driven by the central pacemaker, even though individual olfactory receptor neurons exhibit circadian rhythms independent of the central pacemaker [123]. Circadian pheromonal responses in male turnip moths are not controlled at the antennal level [121].…”