The consequences of eye removal for the circadian rhythm of behavioral activity inAplysia

Summary

TheAplysia eye is capable of both photoreception and circadian oscillation. We have tried to find out if either of these ocular functions plays an important role in controlling the circadian rhythm of locomotor behavior. Eyeless, sham-operated and intactAplysia were tested in LD, DD and pseudo-LD. The behavioral rhythm was measured and analyzed by event recorder techniques supplemented with periodogram analysis.

• 1. In agreement with others we found that (i) intactAplysia were diurnal, (ii) activity onsets frequently occurred slightly before dawn inLD 12∶12 and (iii) a majority of intact animals gave convincing freeruns for up to 2 weeks following release into DD or pseudo-LD (Figs. 1 and 2).

• 2. In intact animals the phase angle difference was more positive in LD 8∶16 than in LD 12∶12 (compare Figs. 1 and 5).

• 3. EyelessAplysia reliably responded to light onset (Figs. 3, 4, and 5). The response persisted for more than 90 days after eye removal (Figs. 3 and 8) and at lighttime intensities of 3 lux or lower (Figs. 7, 8, and 10). Photic responses in eyelessAplysia did not depend on social communication with intact animals (Figs. 9 and 10).

• 4. Even though eye removal did not prevent photic responses, it could have several effects on the daily pattern of activity in LD. These could include (i) an increase in scattered activity during the darktime, (ii) a decrease in activity during the final two-thirds of the lighttime, and (iii) attenuation or elimination of predawn anticipatory activity (Figs. 3, 4, and 5). The third of these effects was by far the most reliable consequence of eye removal in LD.

• 5. Only a minority of eyelessAplysia gave convincing freeruns in DD or pseudo-LD. Nonetheless a few eyeless animals freeran as vigorously as the most vigorous intact ones (compare Fig. 2 with Figs. 3, 4, and 6). We saw eyeless animals in neighboring apparatuses which freeran with distinctly different periods (Fig. 4).

These facts indicate that the eye is neither the only photoreceptor nor the only circadian oscillator coupled to the locomotor rhythm. The eye, however, does participate in the generation of temporal patterns of activity in the absence of h-to-h sensory guidance. It is therefore reasonable to believe that the eye is one among several endogenous oscillators coupled to locomotion. The only role so far demonstrated for the ocular photoreceptors is their previously known capacity to entrain the ocular clock.