Tasty Samples of the Internet for you !
Theme : DreamsREM Sleep in Response to Light and Dark in Congenic Albino and Pigmented F344 RatsWilliam H. Obermeyer and Ruth M. Benca Current Claim: The effects of light on wakefulness and on NREM sleep are similar in congenic albino and pigmented rats, but the effects of light on REM sleep in congenic albino and pigmented rats are different.
To determine whether lights-off triggering is related to albinism in rats, we previously studied (LxBN) F1rats and F2 progeny of (LxBN) and L rats. Only albino F2 rats showed significant increases in REM sleep during brief dark pulses presented during the normal light period. Although albino and pigmented rats strains show differing REM sleep responses to acute lighting changes, their overall sleep-wakefulness responses to light and dark appear to be similar. For example, when living in short light-dark cycles, both L and BN rats obtained more of their NREM sleep during lights-on periods and more of their wakefulness in the dark (Benca et al., 1998). The differing responses of strains of rats to lighting changes suggest that the control mechanisms for REM and NREM sleep are somewhat different. We have recently found that subcortical visual structures, the superior colliculus and pretectum, may be involved in mediating acute responses to lighting changes (Miller et al., 1998b). Albino mammals are known to have anomalous visual pathways (Guillery, 1969; Lund, 1965). It is therefore possible that differences in retinotectal pathways related to albinism may explain differences in REM sleep responses to light. To further explore a possible linkage between albinism and direct effects of light on REM sleep, we report here on a comparison of rats that are congenic at the c locus for albinism. We compared sleep-wakefulness patterns in congenic F344 albino rats that have two copies of the gene for albinism (c/c) and pigmented (hooded) but otherwise identical rats with a single copy of the wild type gene (c/+). These two groups of rats were exposed to standard (LD 12:12) and short (LD 3:3 and 1:1) cycles. Since these animals theoretically differ at only the c locus for albinism, differences in behavioral responses can be attributed specifically to alleles at this location, or albinism.
Lateral EEG, midline EEG, and EMG were recorded beginning no sooner than one week after surgery. The filtered signals were digitized (12 bit, 64 Hz) and the mean of the rectified values for every epoch for each of the signals was saved. All signals were recorded simultaneously on paper to verify the quality of the recordings. Every day each epoch was stage scored using the PASS algorithm as previously described (Bergmann et al., 1987). Computer-generated stage scores were compared to polygraphic recordings to verify the integrity of the system by an individual unaware of the identities of the rats or of LD schedule to which the animals had been exposed. Four albino c/c and 4 pigmented c/+ rats were exposed to three different lighting schedules (LD 12:12, LD 3:3 and LD 1:1) and three illuminance levels (10, 50 and 100 lux measured at the cage floor) yielding nine conditions. Rats were recorded in each condition for at least four days with at least two days accommodation between differing light levels on the same schedule and four days accommodation between different schedules. In addition, two of the pigmented c/+ rats were also tested at 500 lux and 1000 lux. These additional data points are plotted in Figure 1, but were not used in the following statistical comparisons. For each LD schedule and illuminance level, sleep-waking data were averaged for each rat. These averaged sleep and waking variables-percentage of time awake (W%), percentage of time in non-REM sleep (NREM%) and percentage of total sleep time spent in REM sleep (REM/TS)-were evaluated using analysis of variance. The influence of light/dark on the expression of sleep/wake was estimated by the difference between the average value observed in dark and the value of the same variable during the light; i.e., dW=W%Dark-W%Light, dNREM=NREM%Dark-NREM%Light, dREM/TS=REM/TSDark-REM/TSLight. The relationship between the light-dark differences and pigmentation status, schedule and illuminance was evaluated with a general linear model followed by t-tests and Pearson correlations. In all cases light was analyzed as the log10 of illuminance. REM sleep triggering was assessed by comparing average REM/TS for the first five minutes of darkness in either LD 1:1 or LD 3:3 with the average REM/TS for the five minutes immediately preceding dark onset using a paired t-test. Unless otherwise stated, statistical significance was determined using two-tailed tests for t-tests and correlations, =0.05 throughout.
Neither illuminance level nor LD schedule produced a significant change
in overall daily W%, NREM% or REM/TS-all of these parameters remained
very stable across all the combinations of lighting schedule and light
intensities tested (see Table 1). The distribution of sleep between light
and dark periods, however, was markedly affected by both lighting schedule
and lighting intensity (Figure 1). In contrast, REM sleep expression in the light and dark differed markedly between albino c/c and pigmented c/+ rats. Darkness increased REM sleep propensity more strongly and more consistently in albino c/c than in c/+ pigmented rats. This increase in REM sleep propensity was evident in both the tonic difference between REM/TS in the dark and REM/TS in the light (dREM/TS) and in the acute increase in the probability of REM at dark onset (REM sleep triggering). Albino c/c rats had a higher dREM/TS than did pigmented c/+ rats on all LD schedules. Also in albino c/c rats, dREM/TS rose as light intensity increased (although for the LD 1:1 schedule this dose dependency just failed to achieve significance, p=0.06, two-tailed). Albino c/c rats had strong acute REM sleep responses to dark onset-there were immediate, substantial increases in REM/TS (Figure 2). The average REM/TS during the first five minutes of darkness was four times what it had been in the prior five minutes even at 10 lux (LD 1:1). On the LD 3:3 schedule the threefold increase in REM/TS with dark onset at 10 lux did not reach significance, but at both 50 and 100 lux on LD 3:3, the increase in REM/TS was over fifteen-fold and significant. Pigmented c/+ rats displayed a significant tonic increase in REM/TS only on the LD 1:1 schedule. The elevated dREM/TS of the pigmented c/+ rats was statistically significant at the lowest light level (10 lux). This difference between REM/TS during the dark and REM/TS during the light was only about a quarter as great as the corresponding increase in REM/TS in the albino c/c rats, and the difference between the groups of rats was significant. There was a similar trend for REM/TS of pigmented rats to be higher in the dark than in the light at 50 and 100 lux (p<0.11). Pigmented c/+ rats, however, did not have any tonic REM/TS elevation during darkness on the LD 3:3 or LD 12:12. It is also noteworthy that on the baseline schedule (LD 12:12), REM/TS was actually lower in the dark than in the light for pigmented c/+ rats; in comparison, REM/TS continued to be higher in the dark among c/c albinos on this schedule. Brighter light was not associated with higher dREM/TS among pigmented c/+ rats, unlike the pattern seen in c/c albino rats. Pigmented c/+ rats also had a smaller REM sleep triggering response to darkness than did albino c/c rats. The abrupt and substantial increase in REM/TS following lights on among c/c rats was not seen in the c/+ rats (Figure 2). We compared REM/TS in the first 5 min of darkness with REM/TS in the preceding 5 min of light. Except for LD 1:1 at 10 lux, the largest response among pigmented rats was always less than the smallest response among the albino c/c rats. Although there was a tendency for REM/TS to increase at dark onset on the short light:dark schedules in pigmented c/+ rats, this increase was significant only for 100 lux, LD 1:1 during which the responses of the pigmented rats were very small but consistent across animals. The first five minutes of dark for pigmented c/+ rats represented an increase of 4% whereas the increase in albino c/c rats for 100 lux LD 1:1 was nearly dramatically larger (Figure 2). For all other schedules except LD 1:1 at 50 lux, between one (LD 3:3, 100 lux) and three (LD 3:3, 50 lux) of the c/+ rats had lower REM/TS in the first 5 min of dark than during the preceding 5 min of light.
The REM sleep responses of albino and pigmented rats in this study were nevertheless more nearly alike than was the case in the earlier albino-pigmented comparisons. In the current study, the groups of rats were genetically more alike than in any previous comparisons of albino and pigmented rats. It is therefore possible that some of the similarities in the modulatory effects of light and dark on REM sleep in albino and pigmented rats seen in this study could be related either to the overall genetic similarity or to the heterozygous status of the pigmented animals. The effects seen in this study are unlikely to be a result of abnormally high or low light levels. These results were obtained using illuminance levels ranging from 10 to 100 lux which are relatively low and likely representative of those encountered by feral rats, as well as those typically experienced by rats in research settings. Even the lowest of these levels proved to have an effect on the distribution of sleep and wake in both c/c and c/+ animals. It follows that the sleep-wake system of both c/c and c/+ rats was able to respond to light/dark changes of these magnitudes. Neither does it seem likely that the discrepancies in REM sleep are due to differences between groups in overall sensitivity to light or to a difference in activation in response to light or dark. For example, looking at pigmented c/+ rats on the LD 3:3 schedule, W% was higher in the dark than in the light at all levels of illuminance indicating greater activation in the dark than in the light. Furthermore, the size of the dark-light W% difference was nearly as dependent on light intensity in these pigmented c/+ rats as among their c/c albino congenics. Both groups shifted more of their wakefulness to the dark as the intensity of the light increased (as mentioned above, there was no change in 24 h amounts of sleep and wakefulness) suggesting that the underlying process regulating wakefulness was similar, if not identical, between groups. Only in the albino c/c rats, however, did REM/TS in the dark increase along with illuminance. Pigmented c/+ rats showed no relationship of REM/TS to light intensity. Indeed, the only significant difference between light and dark for the pigmented rats in LD 3:3 was at 50 lux when REM/TS was actually lower in the dark than in the light. Whatever mechanism controls the regulation of REM sleep in response to light and dark seems to be acting differently in c/c and c/+ animals, whereas the process connecting light/dark to the overall probability of sleep seems not to be different. This suggests that LD effects on REM sleep and NREM sleep-wakefulness are mediated by somewhat separate systems. Earlier studies (e.g., Deboer and Tobler 1996; van Betteray et al., 1991) also seem to suggest that LD stimuli may be particularly useful in identifying independent sleep components. Separate mediation of REM and NREM sleep is consistent with the observation that the relationship between the expression of REM sleep and NREM can vary markedly from the typical adult pattern, for example, in narcolepsy and during infancy. The relationship between REM and NREM sleep also changes during recovery from extended total sleep deprivation (Everson et al., 1989; Feng et al., 1995). We have recently found that aspiration lesions of the pretectum and superior colliculus eliminate both REM sleep triggering responses and NREM sleep responses to short LD cycles (Miller et al., 1998a). Selective neurotoxic lesions of the pretectum, on the other hand, eliminate REM sleep triggering to lights-off (unpublished observations), but do not appear to reduce the effects of short LD cycles on patterns of sleep-wakefulness (Miller et al., 1998b). Exploration of the systems underlying light-dark responses of overall sleep-wake and REM sleep can be difficult when the responses closely parallel one another, as they do in many strains. Differences between the systems regulating sleep responses to light and dark are accentuated in some, to date mostly albino, rat strains. The current study exploited the accentuated difference seen in albino rats in order to discern one of the factors contributing to the mechanism controlling the REM sleep response to light and dark. The alleles at (or near) the c locus, or albinism per se, seem to be implicated specifically in the control of REM sleep by light and dark, since light and dark affected REM sleep expression differently in albino c/c vs. pigmented c/+ congenic rats. This is not to say that albinism is, by any means, the sole factor determining regulation of REM sleep by light. For example, we have previously shown that pigmented BN rats show decreased REM/TS during the dark periods in a short LD cycle (Benca et al., 1998), although this is in the opposite direction from albino rats. In the present study, F344 c/+ pigmented rats were more likely to have REM sleep during their sleep in the dark on the LD 1:1 schedule, although the effect was small. Even though the data obtained at higher light levels (500 and 1000 lux) and on the LD 3:3 schedule did not show increases in REM/TS in the dark, they do not rule it out. Thus, light and dark can have acute effects on REM sleep expression in both albino and pigmented rats, although these responses may be different. Our results demonstrate that the direct influence of light and dark on REM sleep in rats is likely related to the c locus, which controls albinism, or to albinism itself. We cannot, with absolute certainty, rule out the possibility that loci immediately adjacent to the c locus are also involved in sleep regulation, but this is unlikely. The system underlying the direct influence of light and dark on NREM sleep and on overall sleep-waking behavior, on the other hand, appears to be relatively independent of the c locus or albinism.
3. Benca RM, Obermeyer WH, Bergmann BM, Lendvai N, Gilliland MA. Failure to induce rapid eye movement sleep by dark pulses in pigmented inbred rat strains. Physiol Behav 1993; 54(6): 1211-4. 4. Benca RM, Overstreet DE, Gilliland MA, Russell D, Bergmann BM, Obermeyer WH. Increased basal REM sleep but no difference in dark induction or light suppression of REM sleep in Flinders rats with cholinergic supersensitivity. Neuropsychopharmacology 1996; 15(1): 45-51. 5. Bergmann BM, Kushida CA, Everson CA, Gilliland MA, Obermeyer WH, Rechtschaffen A. Sleep deprivation in the rat: II. Methodology. Sleep 1989; 12: 5-12. 6. Bergmann BM, Winter JB, Rosenberg RS, Rechtschaffen A. NREM sleep with low-voltage EEG in the rat. Sleep 1987; 10: 1-11. 7. Borbely AA. Sleep and motor activity of the rat during ultra-short light-dark cycles. Brain Res 1976; 114: 305-17. 8. Borbely AA, Huston JP, Waser PG. Control of sleep states in the rat by short light-dark cycles. Brain Res 1975; 95: 89-101. 9. Deboer T, Tobler I. Shortening of the photoperiod affects sleep distribution, EEG and cortical temperature in the Djungarian hamster. Journal of Comparative Physiology A-Sensory Neural & Behavioral Physiology 1996; 179(4): 483-92. 10. Everson CA, Gilliland MA, Kushida CA, Pilcher JJ, Fang VS, Refetoff S, Bergmann BM, Rechtschaffen A. Sleep deprivation in the rat: IX. recovery. Sleep 1989; 12: 60-7. 11. Feng P-F, Shaw P, Bergmann BM, Obermeyer WH, Tsai LL, Zenko CE, Rechtschaffen A. Sleep deprivation in the rat: XX. Differences in wake and sleep temperatures during recovery. Sleep 1995; 18(9): 797-804. 12. Guillery RW. An abnormal retinogeniculate projection in Siamese cats. Brain Res 1969; 14: 739-41. 13. Johnson JH, Adler NT, Sawyer CH. Effects of various photoperiods on the temporal distribution of paradoxical sleep in rats. Exp Neurol 1970; 27: 162-71. 14. Lisk RD, Sawyer CH. Induction of paradoxical sleep by lights-off stimulation. Proc Soc Exp Biol Med 1966; 123: 664-7. 15. Lund RD. Uncrossed visual pathways of hooded and albino rats. Science 1965; 149: 1506-7. 16. Miller AM, Obermeyer WH, Behan M, Benca RM. The superior colliculus mediates the direct effects of light on the timing of sleep in albino rats (abstract). Sleep 1998a; 21(Suppl): 22. 17. Miller AM, Obermeyer WH, Behan M, Benca RM. The superior colliculus-pretectum mediates the direct effects of light on sleep. Proc Natl Acad Sci U S A 1998b; 95(15): 8957-62. 18. Tobler I, Borbely AA. Enhancement of paradoxical sleep by short light periods in the golden hamster. Neurosci Lett 1977; 6: 275-7. 19. Tobler I, Borbely AA. Short light dark cycles and paradoxical sleep in the rat: effect of strain difference and hypophysectomy. Behav Biol 1978; 23: 395-8. 20. Van Betteray JNF, Vossen JMH, Coenen AML. Behavioural characteristics of sleep in rats under different light/dark conditions. Physiol Behav 1991; 50: 79-82.
Original address of this text : |