Photoperiodic Effects On Thermoregulation in A ‘Blind’ Subterranean Mammal

The effect of changes in the 24 h photoperiod on the thermoregulatory capacity of rodents has been critically studied (Lynch, 1970; Heldmaier, Steinlechner, Rafael & Vsiansky, 1981). It has been demonstrated recently that short photoperiod (8L: 16D) increased the resistance of Apodemus mystacinus upon exposure to low ambient temperature (T_a) of 6 °C (Haim & Yahav, 1983).

In adult mammals the retinal components of the visual system are the only parts known to be involved in the mediation of the effect of light on the pineal gland (Martin, 1976). While both the receptors for pineal regulation and visual perception are located in the retina, the neural pathways from the retina to the effectors are distinct in the two systems.

The subterranean mole rat Spalax ehrenbergi is considered to be a blind rodent (Cei, 1946), presumably associated with its underground lifestyle (Nevo, 1979). Pevet, Kappers & Nevo (1976) studied the ultrastructure of the pinealocytes of S. ehrenbergi and compared the results with those of the subterranean mole Talpa europea. They suggested that the mole rat cannot detect changes in ambient light.

This study was conducted in an attempt to explore the thermoregulatory response to changes in photoperiodicity.

Mole rats, Spalax ehrenbergi, of both sexes (112–234 g), which were found to be cold sensitive when acclimated to a daily light regime of 12h light: 12h dark (12L: 12D), at T_a = 22 °C (Haim, Heth & Nevo, 1983), were used in this study. They were kept individually in cages and fed fresh vegetables.

Potentials were recorded from six mole rats, Spalax ehrenbergi, and one control rat, Rattus norvegicus (Berkenhout). Animals were anaesthetized by intraperitoneal injection of Sagatal (May & Baker 85 mg kg⁻¹ body weight). To prevent shivering the animal’s body temperature was maintained by warming.

Brief (10 μs) flashes from a flash tube with approximately 1 500000 candle power were delivered to the under-integument eyes, from a distance of 30 cm. Flashes were delivered at a rate of 2 s⁻¹ and the sound generated by the discharge of the flash tube was masked by white noise from a speaker mounted on the flash tube stand behind the tube. Sub-dermal needle electrodes were inserted on the forehead, at the occipital region and on the back. Differential amplification (×100000) of the potentials recorded between the occipital and the forehead electrodes was performed at a band-pass of 3–1000Hz (3 DB down points, 6DB/octave slope). The potentials were averaged over a 256 ms period, using a dwell time of 1000 /is and 256 addresses per record. Responses to 200 stimuli were averaged to produce each trace and a duplicate of each average was made to assess reproducibility. The averaged potentials were stored on magnetic tape for further analysis. Potentials were displayed on a CRT screen, with positivity at the occipital electrode as an upward deflection. Latencies and amplitudes of peaks were determined from the computer by the cursor. Latencies were measured relative to the flash-synchronous trigger to the computer, and amplitudes were measured between peaks and the subsequent throughs.

Mole rats acclimated to 12L: 12D at T_a = 22 °C (group A) were hypothermic when exposed to T_a = 6 °C for 6 h. In contrast, acclimation of mole rats to a photoperiod of 8L: 16D at T_a = 22°C (group B) caused a significant increase in resistance to cold. Body temperature (Tb) after 6h of exposure to cold was 35·9 ± 0·55 °C, an increase of 1·6 °C compared to the previous group (Table 1 ). The mean T_b in group B did not change upon exposure to cold, while in group A, T_b fell by 2·1 °C (P<0·001). A significant (P< 0·01) difference was found in the decrease of body weight (W_b) during the exposure to cold between group B (a mean loss of 4·9 ± 1·9%) and group A (9·3 ± 4·5%). The transfer of the mole rats from 8L: 16D (group B) to 12L: 12D but at T, = 17 °C (group C) did not cause a decrease in ΔT_b (the difference in T_b between the beginning of exposure to T_a = 6°C and at the end of the exposure). There was, however, a significant increase in the loss of W_b in mole rats of group C (7·7 ± 2·7%) compared to group B (4·9 ± 1·9%). The acclimation of mole rats to 16L: 8D at T_a = 17 °C (group D) caused a significant decrease in resistance to cold. T_b in these individuals after 6h of exposure to T_a = 6°C dropped to 34·6°C (Table 1) and these individuals lost 8·8 ± 2·7% of their body weight.

Fig. 1 compares the visually-evoked potentials from a laboratory rat and from one of the mole rats. The evoked potentials recorded from the mole rats did not show any comparable component that could be consistently recorded. The signals detected were usually under 1 μV amplitude and were not reproducible between repetitive recordings from the same animal. In contrast, evoked potentials in the rat included a sharp initial component at 35 ms and a subsequent component peaking at 120 ms followed by a number of later peaks. The amplitudes of these components were in the order of a few μV.

The results suggest that no response from the visual pathway of the mole rat, as evaluated by visual-evoked potentials, could be detected by flash stimuli. In contrast, using the same recording parameters, clear potentials could be recorded from the laboratory rat in our recording (Fig. 1) (see also Schwartzbaum, Ide-Johanson & Belgrade, 1974). Mole rats can thus be considered to be effectively blind. Nevertheless, mole rats responded to photoperiod changes (Table 1), as evidenced by their thermoregulatory capacity. Therefore, other channels should be considered. The involvement of the pineal organs in thermoregulation of vertebrates was reviewed by Ralph, Firth, Gren & Owens (1979). They suggested that melatonin could be the hormone mediating thermal responses to changes in photoperiodicity in adult mammals. It has been shown that in adult mammals only the retinal components of the eyes contribute to physiological mediation of changes in light on the pineal gland (Moore & Klein, 1974; Martin, 1976). Furthermore, the destruction of primary tract fibres may have no influence on pineal rhythms, which are maintained even when animals are blinded by cutting the primary optical tracts. The ‘blindness’ of the mole rat Spalax ehrenbergi was studied by Cei (1946). In this study it was found that an atrophied retina exists in the rudimentary eye of this species, situated under the integument.

The present results show that transfer to short photoperiod (8L: 16D) without changing ambient temperature (22°C), caused a significant increase in the resistance of the mole rat to cold. Yet a drop of 5 °C in ambient temperature and an extension of the photoperiod to 16L: 8D decreased the resistance to cold significantly.

An increase in heat production was observed in a diurnal rodent as well as in a nocturnal rodent acclimated to short photoperiod (Haim & Fourie, 1980). The same results were obtained by melatonin treatment in these species (Haim & Fourie, 1982). These results support the general hypothesis that the pineal gland, via melatonin, can be a mediator in environmental photoperiod changes. The existence of the rudimentary retina in the mole rat and the fact that the neural pathways utilized from the retina to the effectors are separated does not rule out the involvement of the atrophied eye. In his study on the functional morphology of the vertebrate visual system Ulinski (1980) recognized three nested levels of organization within the visual system: neurones, modules and network. The results of our study suggest that the network level of the mole rat is non-functional. However, the function of modules and neurone levels are to be further studied.

It has been suggested that the harderian gland is involved in the visual system through its porphyrine content (Wetterberg, Geller & Yuwiler, 1970). It was also shown that removal of the harderian gland in hamsters resulted in a decrease of melatonin content in the pineal gland (Panke, Reiter & Rollag, 1979). Balemans, Pevet, Legerstee & Nevo (1980) studied the synthesis of melatonin in the pineal gland, retina and harderian gland of the mole rat. They raised the question of pineal metabolism regulation in eyeless mice and in rodents with atrophied eyes. They suggested that the indole metabolism in the harderian glands of the mole rat may be responsible for the indole metabolism in the pineal gland. However, they did not rule out the regulation by temperature as was suggested by Nir & Hirschmann (1978).

We suggest that the ‘blind’ mole rat may detect changes in photoperiod through its atrophied eyes or via some other mechanisms which involve the melatonin pathway. The involvement of the harderian gland and other neural pathways are currently under study. The ‘blind’ mole rat appears, therefore, to be an ideal test organism for illustrating the mechanisms and neural pathways connected with mediation of photoperiodicity.

We thank Dr U. Katz for critically commenting on the manuscript and Professor G. Heldmaier and Dr M. Stoddart for their helpful remarks. We also thank Ms B. Frooman and Mr S. Samson for their technical assistance.