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Circadian regulation of olfactory receptor neurons in the cockroach antenna - PubMed

Circadian regulation of olfactory receptor neurons in the cockroach antenna

A S M Saifullah et al. J Biol Rhythms. 2009 Apr.

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 EAG and the activity of olfactory receptor neurons (ORNs) in single olfactory sensilla were recorded simultaneously for 3 to 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.

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Figures

Fig. 1
Fig. 1

Shows stability over time of recordings from a cockroach antenna. In each record, the top trace shows impulse activity from a single olfactory sensillum while the bottom trace records the EAG from the same antenna. A, is the recording at 1 hour; B, 48 hours; and C, 96 hours after the recording was begun. Stimulus in all cases was a 1.5 second pulse of ethyl acetate. The stimulus artifact (arrow) marks the onset of the stimulus.

Fig. 2
Fig. 2

Circadian oscillations in the number of action potentials and EAG amplitude recorded from cockroach antennae in response to a standard pulse of ethyl acetate given once per hour. A and B plot the number of spikes recorded from a single olfactory sensillum and the EAG amplitude recorded from the same antennae. Animals were isolated in DD for the duration of the recording. The phase of the dark period of the prior light cycle (LD 12:12, lights on at 20:00 CST) is shown as a black bar on the first day. Both ORN activity and EAG amplitude exhibit circadian rhythms that freerun in constant darkness. C, D show the average, ORN activity (N=6) and EAG amplitude (N=5) following normalization with respect to maximum values. Error bars are standard errors that for clarity are only shown in the upward direction. Peak activity in both the ORNs and EAG occur in the early subjective day. E, shows the relative changes in mean amplitude of the largest spike in each hourly record over the first two days of recording. Over the 48 hour period, spike amplitude falls, on average, by about 20%, but there are no time-of-day effects.

Fig. 3
Fig. 3

Entrainment of ORN and EAG rhythms. Circadian oscillations in spike counts and EAG amplitude recorded in DD from animals that had been entrained to LD 12:12 (lights on at 08:00) shifted 12 hours from the light cycle used to entrain the animals from Fig. 2. A, B show data plotted from a single individual. C, D show average, normalized activity in ORNs (N=6) and EAGs (N=7) recorded from 7 animals. Peak activity is again in the early subjective day for both ORN and EAG rhythms.

Fig. 4
Fig. 4

Correlation between EAG amplitude and ORN response. A and C, plots of EAG amplitude (solid lines) and spikes (open circles) in response to hourly pulses of ethyl acetate. B and D, plots of the number of spikes as a function of EAG amplitude. Spikes and EAG are correlated, but there is significant variability. E, examples of ORN recordings at 48 hours and 96 hours for the antenna from C – only the large unit was counted.

Fig. 5
Fig. 5

Effects of severing the optic tracts on rhythms in ORN response and EAG amplitude. Recordings were made in DD 7–10 days after surgery. A, B show data plotted from a single individual while C, D show average, normalized activity in ORNs recorded from 4 animals. Despite the loss of rhythmicity in EAG amplitude the response of the ORNs persisted after surgery. The results indicate that the circadian rhythms in EAG and ORN responses are controlled by anatomically separate circadian mechanisms.

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