filogenia del sueño

7/29/2019 Filogenia del sueo

1/14

1630-8493-1519-0/05/$0.00+$1.50 2005 by CRC Press LLC

9 Sleep Phylogeny:Clues to the Evolutionand Function of Sleep

Jerome M. Siegel

CONTENTS

Introduction............................................................................................................163Terrestrial Mammals..............................................................................................164

Aquatic Mammals..................................................................................................168

Reptiles ..................................................................................................................171

Conclusions............................................................................................................174

References..............................................................................................................174

INTRODUCTION

A persuasive argument for the importance of sleep rests on its ubiquity among

animals. All mammals sleep.

1

Reptiles appear to sleep, although by some measures

they may not.

29 It has not been conclusively demonstrated that fish sleep, although

some species show marked circadian rhythms of activity.

10,11 To meet the accepteddefinition of sleep, animals must show periods of inactivity with raised arousal

thresholds and must show sleep debt

when deprived, leading to rebound sleep when

deprivation is ended. Fruit flies (

Drosophila melanogaster

) show periods of inactivity

with raised arousal thresholds and sleep rebound after deprivation.

1214

If such periods

are homologous to sleep in vertebrates, one must consider any reported absence of

sleep in higher vertebrates as an error due to inadequate assessment or to be an

evolved adaptation to particular ecological niches that has done away with a sleep

state present in ancestral animals. This chapter discusses the special situation of

marine mammals, which appear to have evolved adaptations that at the very least

mask some aspects of sleep and certainly dispense with the need for immobility

during what otherwise appears to be sleep. A further issue is the nature of sleep. Most

mammals

1,15

and birds

16

show evidence of REM sleep also known as paradoxical

sleep (PS) although this state may not exist in certain marine mammals.

17

Amounts of sleep differ substantially between species, with some sleeping as

little as 2 h per day and others as much as 20 h.

1,15

Surely these enormous variations

1519_C09.fm Page 163 Tuesday, August 24, 2004 2:02 PM


2/14

164

Sleep: Circuits and Functions

offer some insight into the physiological needs responsible for sleep. Although

animals in different ecological niches might most adaptively have evolved differingdurations of activity and inactivity, it is unlikely that no animals would have evolved

a complete or nearly complete absence of sleep unless it served some vital function.

The cost of sleep in terms of vulnerability, loss of time to eat, procreate, and gain

an edge in competition with other animals is considerable. Certainly contemporary

humans make major efforts to reduce sleep time to achieve their goals. Differences

in sleep amounts seem to be systematically related to certain constitutional variables,

suggesting that underlying physiological factors, rather than ecological niche, deter-

mine sleep need. The study of sleep phylogeny can help explain the essence of sleep

debt; i.e., which physiological, neurochemical, and genetic events are conserved

across sleep in differing animals.

TERRESTRIAL MAMMALS

Although there are approximately 4,000 mammalian species, fewer than 100 have

been studied under laboratory conditions. Most of these have been observed in only

a single study. Perhaps an additional 100 have been observed in zoos. Certainly there

is no need to study sleep in all mammalian species; however it is likely that a thorough

examination of sleep physiology, exploring the genetic variations and adaptations

that have occurred over more than 100,000,000 years of mammalian evolution, may

reveal aspects of sleep not seen in the four or five laboratory species that have been

most thoroughly studied. For example, humans and rats have been shown to have a

clear link between REM sleep and penile erections.

16,19

A recent study of sleep in

the armadillo revealed that penile erections occur in non-REM sleep, but not in REM

sleep in this species.

20

Such observations are not merely a curiosity but speak to the

issue of which aspects of sleep are core phenomena and which are perhaps epiphe-

nomena not linked to particular sleep-waking states. In this case, the findings suggest

that certain aspects of sympathetic and parasympathetic control during sleep differ

across species. One may speculate that other aspects of standard sleep signs in rats,

cats, and humans, such as high voltage electroencephalogram (EEG) during non-

REM sleep, low voltage EEG during REM sleep or high voltage EEG occurring

simultaneously in both hemispheres, may not be essential for sleep. Many of the

largest mammals such as elephants, and giraffes have only been studied by visual

observation. Understanding sleep in these animals is crucial, because the extreme

points in any cross species comparison can be most informative as to the underlying

variables that determine sleep amounts and physiology.

Perhaps the most surprising conclusion from studies of mammalian sleep is that

knowing the order to which an animal belongs tells you very little about the amount

of total sleep or REM sleep they have.

1,15

In other words, as a group rodents do nothave characteristic sleep patterns that differentiate them from carnivores, primates,

artiodactyls, insectivores, and so on. Each of these groups shows a wide and over-

lapping range of total and REM sleep amounts. Each order is characterized by a

common genetic inheritance that produces characteristic behaviors, brain and body

anatomy, intelligence, diet, and reproductive physiology that tends to differentiate

it from other orders. Yet their sleep is not characteristic of the group, suggesting that



3/14

Sleep Phylogeny: Clues to the Evolution and Function of Sleep

165

these variables do not determine sleep amount. A comprehensive analysis of the

determinants of sleep time looking at body weight, metabolic rate, brain weight,encephalization quotient (brain-to-body weight ratio), body temperature, neonatal

brain weight as a percentage of adult weight, gestation period, and litter size con-

cluded that total sleep time was most closely correlated with body weight

15

(Table

9.1). This was a negative correlation; i.e., big animals sleep less. Body weight is

inversely related to metabolic rate, so we can say that animals with higher metabolic

rate have more total sleep time. The implications of this is discussed in the Conclu-

sions section.

Among terrestrial mammals REM sleep amounts are positively correlated with

total sleep amounts; however this explains only a small amount of the total variance

in REM sleep time. It has been noted that predator animals and animals with safe

sleeping sites have relatively larger amounts of REM sleep.

21

This makes some sense,

because arousal thresholds are elevated in some animals in REM sleep, so it might

be dangerous for prey animals to have large amounts of REM sleep., It is not true,

however, that REM sleep is deep sleep in all animals.

22

In humans, for example,

arousal from REM sleep is more rapid than from non-REM sleep, and there is

evidence that in general animals aroused from REM sleep function better than those

aroused from non-REM sleep.

23

It is difficult to quantify safety of sleep site by

measures such as frequency of death during sleep. Sites that seem exposed may in

fact be safe, and there is little evidence that animals are disproportionately hunted

during sleep. Therefore, while there is little doubt that certain predator animals have

large amounts of REM sleep, this relation does not appear to adequately explain

REM sleep time.

An alternate correlate of REM sleep time is how immature animals are at birth.

At birth all mammals so far examined have their maximal amounts of REM sleep.

Amounts diminish with age to adult levels.

24

Animals such as rats or cats that areborn relatively immature have a greater elevation in REM sleep at birth. Animals

such as horses or guinea pigs that are born relatively mature have little elevation

of REM sleep at birth. This suggests that REM sleep may have some role in brain

or body development or in the protection of small animals without substantial

thermoregulatory capacity from hypo- or hyperthermia. This role has not been

identified. Furthermore, even though animals that are immature at birth have

TABLE 9.1Correlations between Sleep Parameters and Constitutional Variables

Total DailySleep Time

Quiet SleepTime

REM SleepTime

REMSleep%

Sleep CycleLength

Body weight

0.53

a

0.53

a

0.45

a

0.12 0.83

a

Brain weight

0.55

a

0.48

a

0.52

a

0.25 0.89

a

Metabolic rate 0.33

b

0.30

b

0.13

0.09 0.82

Encephalization quotient

0.17

0.10

0.20

b

0.30

b

0.52

b

a

P


4/14

166


decreasing REM sleep amounts as they age, they continue to have higher REMsleep amounts when they reach adulthood (Table 9.2

24

). No theory has been offered

as to why this is; however, from a statistical standpoint, the correlation between

immaturity at birth and REM sleep time in adulthood accounts for a large amount

of the interspecies variability in REM sleep time between mammals. Figure 9.1

25

shows some mammals with relatively high and low amounts of REM sleep. It is

important to note that humans do not have unusual amounts of REM sleep either

in terms of the number of hours per day or the percent of sleep time devoted to

REM sleep (Figure 9.1); rather the amount of REM sleep time shown by humans

is in line with our intermediate state of maturity at birth. This is obviously a problem

for any theory hypothesizing that REM sleep amount is linked to intellectual capac-

ity or any other characteristic in which humans are believed to be at an extreme

within the animal kingdom.

25

The monotremes are one of the three branches of the mammalian line, the othertwo being the placentals and the marsupials.

1

The extant monotremes are the short-

and long-nosed echidna and the platypus. The monotremes are egg-laying mammals

that have relatively low but regulated body temperature (approximately 32

C). They

nurse their young from milk-secreting patches, rather than nipples and have thick

fur. Their bone structure contains some reptilian characteristics, and genetic analysis

indicates that they are more similar to reptiles and birds than other mammals. The

platypus has a bill that responds to electric fields and a poison spur, characteristics

typically seen in reptiles or fish but not in mammals. Despite the origin of

monotremes early in the mammalian line, relatively little speciation has occurred,

with only five monotreme species known to have evolved, presumably because their

geographic isolation from other species reduced evolutionary pressure.

1

Thus the

physiology of monotremes is likely to more closely resemble that of the first mam-

mals than any other mammals, and an early report that echidnas did not have REMsleep generated considerable interest.

26,27

It suggested that REM sleep was a more

recently evolved state with some higher cognitive function.

Because of the possibility that a REM sleep-like state might be missed in the

echidna, we reexamined this issue. In addition to recording electroencephalograms

and electromyograms, we monitored brainstem neuronal activity.

28

We know that

TABLE 9.2Correlations of REM Sleep Parameters with Measures of

Neonatal Maturity and Reproductive Variables

REM SleepTime

REM Sleep% of TotalSleep Time

Altricial-precocial rating

0.66

a

0.45

b

Neonatal brain weight (% adult)

0.61

a

0.55

b

Litter size 0.51

a

0.41

b

a

P


5/14


167

FIGURE9.1

TotalsleepamountsandREM

sleepamounts.Hu

mansarenotunusualeitherintermsoftheirtotalsleeporREM

sleepamounts.(F

rom

SiegelJ.M.,TheREM

sleep-memoryconsolidationhypothesis,

Science

,294,10581063,2001.Withpermission.)



6/14

168


brainstem neuronal activity generates REM sleep

29

; therefore it might be possible

to detect a REM sleep-like state in the echidna even if the forebrain EEG did notresemble that of REM sleep in placental mammals. We found that brainstem activity

during sleep in the echidna did not resemble the activity seen in other mammals

during non-REM sleep. Rather it resembled that seen in REM sleep (Figure 9.2).

We concluded that echidnas did have a REM sleep-like state, but one that was not

accompanied by low voltage cortical EEG as is seen in adult mammals. In this

respect the REM sleep-like state resembled that of many neonatal animals, which

have high voltage activity during periods of REM sleep. It has also been reported

that a state looking like REM sleep, with low voltage EEG, may occur in echidnas.

30

We saw no such state in our studies, and the Nicol et al. study did not demonstrate

that the state they were observing was a sleep state, rather than a quiet waking state,

so further investigation of this issue may be warranted. Both studies agree, however,

that the echidna has a REM sleep-like state, in contrast to the earlier work.

Because we saw a state that resembled REM sleep in the echidna, we nextstudied sleep in the platypus, which is considered the most primitive of the mam-

mals.

31

This raised special problems, because these animals are very delicate, are

dangerous to handle because of their poison spurs, and are partially aquatic and

cannot be housed in conventional cages. The platypus requires special animal hus-

bandry procedures. Water pumps, needed to circulate water in their pool, generate

large electrical fields, which stress and thereby can cause the death of the animals.

Shielding procedures have to be used to minimize this stimulus. Telemetry, both on

land and under water, is necessary to allow continuous recording. When we suc-

ceeded in recording from the platypus, we found that it has a particularly vigorous

motor activation during sleep, equal to or greater than that of other mammals in

REM sleep (Figure 9.3). A video of this can be viewed at our web site http://www.

npi.ucla.edu/sleepresearch. When we calculated the amount of REM sleep, we were

surprised to discover that the platypus had more REM sleep than any other animal,

up to 8 hours per day. Both the echidna and platypus are extremely immature at

birth, resembling a worm. They crawl out of the birth canal and into a pouch where

they are protected, warmed, and nourished for several months. The high levels of

REM sleep in monotremes strengthen the relation between immaturity at birth and

REM sleep amounts in adulthood.

AQUATIC MAMMALS

Aquatic mammals have sleep patterns that are quite different from those in terrestrial

mammals, so investigation of sleep in marine mammals may be instructive in under-

standing sleep as a whole, as well as the role of REM versus non-REM sleep.

Under some conditions dolphins swim 24 hours a day for long periods. Duringtheir swimming they breathe regularly and are able to avoid the sides of the pool.

Lilly first noticed that dolphins often close one of their eyes but rarely close both.

The significance of this was discovered by Lev Mukhametov and colleagues, who

developed reversible, relatively noninvasive techniques for recording EEG during

swimming. They found that dolphins generated the high voltage EEG typical of non-

REM sleep in either the right or left side of their cortex, but never in both sides.

32



7/14


169

FIGURE9.2

Instantaneousrateplotsofmedialreticularneuro

nsduringsleepandwakingstates.Inthe

echidna,ratevariesinawayresembling

that

seeninplacentalmam

malsduringREM

sleep,ratherthanthat

intheregularmannerofnon-REM

sleep

.(FromSiegelJ.M.,MangerP.,NienhuisR.,

FahringerH.M.,PettigrewJ.,Theechidna

Tachyglossusaculea

tus

combinesREM

andnon-REM

aspectsinasinglesleepstate:implicationsforthe

evolutionofsleep,

J.Neuroscience

,16,35003506,1996.With

permission.)



8/14

170


The same unihemispheric sleep has now been seen in several cetacean species.

33

Figure 9.4 shows an EEG recording we carried out in a beluga whale. USWS appears

to be at least partially an adaptation to the complex brain activity required for

breathing in the dolphin. In contrast to other animals that breathe automatically during

sleep, dolphins and other cetaceans need to be at the surface to breathe, need to sensewave action, and minimize water ingestion during breathing movements. Adminis-

tration of light doses of barbiturates to dolphins will stop breathing (long before it

produces effective analgesia). This is quite different from terrestrial mammals that

breathe and regulate blood gasses effectively even when deeply anesthetized.

In the dolphin the optic chiasm is completely crossed so that all visual input to

each hemisphere comes from the opposite eye. Because visual input can block certain

FIGURE 9.3

Sleep states in the platypus. The platypus has periods of rapid eye movements

during a state characterized by high voltage EEG. (From Siegel J.M., Manger P.R., Nienhuis

R., Fahringer H.M., Shalita T., Pettigrew J.D., Sleep in the platypus, Neuroscience

91,

391400, 1999. With permission.)



9/14


171

EEG rhythms,

34

it is necessary to determine if any EEG change observed contralat-

eral to a closed eye is secondary to the reduction of visual input. Generally the eyecontralateral to the hemisphere that was sleeping was closed, as one would expect,

because it is unlikely that visual input could be effectively processed in the hemi-

sphere with EEG synchronization; however we also demonstrated that eye closure

was not the cause of the high voltage EEG Closure or covering of one eye did not

necessarily produce high-voltage activity in the opposite hemisphere. Conversely

we noted that the eye opposite the sleeping hemisphere could open without blocking

the high voltage EEG

33

; therefore the EEG-defined sleep state is not simply a

consequence of reduced visual input to the contralateral eye. A similar control for

vision-related EEG changes has not been done to support claims of USWS in birds,

who in any case show relatively subtle differences between the EEG in the two

hemispheres, consistently detectable only with power spectral analysis,

35

in contrast

to the USWS visible in cetaceans. If one hemisphere is prevented from showing

high-voltage EEG by gently stimulating dolphins, a rebound of sleep in the deprivedhemisphere is seen when deprivation stops,

36

important evidence that sleep debt can

be localized to one hemisphere.

Despite many studies, no convincing evidence of REM sleep in dolphins or any

other EEG instrumented cetacean has been produced. The absence of such evidence

may result from the conditions under which these observations have been made.

Often the animals are restrained during recordings. In those cases where they have

been unrestrained, the stimulation caused by the recording cable may have prevented

appearance of REM sleep but, considering the strong REM sleep pressure shown by

all terrestrial mammals that have been deprived and that allows high levels of REM

sleep even under uncomfortable sleeping conditions, one would expect that some

unequivocal REM sleep would have been seen even under less than natural condi-

tions. One can conclude that if REM sleep exists in the dolphin, REM sleep amounts

are among the smallest of any mammal or are uniquely sensitive to disturbance.

A more subtle issue is whether REM sleep may take some novel form in dolphins

that has escaped detection. An alternate hypothesis is that unihemispheric slow-wave

sleep may eliminate the need for REM sleep; for example, if REM sleep has evolved

to stimulate brainstem areas after non-REM sleep to allow optimal functioning in

subsequent waking, the presence of virtually continuous brainstem activity required

for the continuous movement and breathing shown by dolphins may make REM

sleep unnecessary.

REPTILES

The presence of REM sleep in large amounts in the most primitive mammals and

in birds suggests that it may have been present in a common ancestor of these twoclasses of animals. That would indicate that at least some reptiles have REM sleep.

The alternate theory, that REM sleep evolved twice, once in mammals and once in

birds, suggests that a REM sleep precursor state must have existed in pre-avian,

premammalian reptiles. According to both hypotheses, examination of state organi-

zation in reptiles would provide an insight into the primitive aspects of REM sleep.

The key challenge is devising a method that would be effective in detecting such a



10/14

172


state. To do this we decided to follow the approach we used in the echidna. Because

we knew what the pattern of brainstem neuronal activity is in the mammalian REMsleep state, and because midbrain and pontine brainstem regions are both necessary

and sufficient for generating the major neurological changes seen in REM sleep,

29

we decided to conduct the first investigations searching for aspects of REM sleep

at the neuronal level in reptiles.

37

We chose the turtle as a representative reptile

because excellent prior behavioral studies had been conducted on these animals

7

and

because they adapted well to the laboratory.

FIGURE 9.4



11/14


173

At the neuronal level, there are two consistent brainstem activity changes under-

lying REM sleep. One is the burst-pause discharge pattern that gives rise to the rapideye movements and twitching characteristic of REM sleep. This pattern is present

in most medial reticular neurons and therefore should be relatively easy to detect.

The second is the cessation of release of norepinephrine, serotonin and histamine

during REM sleep. This would be much more difficult to detect, because these

monoaminergic cell groups are intermingled with other cell types and there is no

easy way to determine the transmitter phenotype of any recorded cell. Our immu-

nohistochemical analyses showed, however, that these cell groups were present in

the turtle, so we focused our effort on recording neuronal activity from medial

reticular cells during quiescent states, expecting to record from non-monoaminergic

and possibly monoaminergic cells.

Our results were clear. We saw no acceleration of discharge and no burst-pause

pattern of discharge analogous to that seen in mammalian reticular cells during sleep.

It appears that this aspect of REM sleep is not present in any form in turtles. Wedo not know the pattern of discharge of monoamine cells in the sleep of the turtle,

and it is possible that a cessation of discharge occurs during behavioral immobility.

However, we did not see cells that had the tonic waking discharge with cessation

of discharge within the sleep period even though some of the neurons we recorded

were within the serotonergic raphe region. Further investigations are necessary to

test for this possibility. What we can conclude is that the periodic occurrence of

brainstem activation that is so characteristic of REM sleep in terrestrial mammals

is absent in the turtle. REM sleep precursor states may be present in the reptilian

species that gave rise to mammals and birds but not in modern day turtles. Alterna-

tively the phasic motor activation seen in REM sleep may have evolved rapidly at

the onset of the avian and mammalian lines, perhaps in relation to homeothermy.

FIGURE 9.4

(See facing page.) Relationship between EEG and the state of eyes in a beluga

whale. (A)

The state of eyelids and EEG spectral power (13 Hz; 5-sec epochs) from the two

hemispheres (R, right; L, left) in a white whale recorded over a 3-h period. EEG power was

normalized as a percentage of the maximal power in each hemisphere during this period. The

state of each eye (R, right; L, left) was scored in real time (O, open; I, intermediate; or C,

closed) and then categorized for 5-sec epochs as described. Compressed figure does not show

short-lasting changes in eye state. (B)

Expansion of the two 2.5-min recordings of the EEG

and the state of both eyes. The examples show the EEG asynchrony and parallel changes in

eye state recorded in this whale at the times marked as 1

and 2

in Figure 4 A

. Note that the

EEG does not change immediately with changes in eye position. The right eye did not close

during episode 1, and the left eye did not close during episode 2. (C)

The average EEG

spectral power in the two hemispheres during episodes with unilateral eye opening (LO/RC,left open and right closed; LC/RO, left closed and right open). EEG power was normalized

as a percentage of the average 13 Hz power recorded in each hemisphere during SWS with

the contralateral eye closure. Reported values are the means S.E. (LO/RC, n = 238 epochs;

LC/RO, n = 441 epochs). (From Lyamin, O.I., Mukhametov, L.M., Siegel, J.M., Nazarenko,

E.A., Polyakova, I.G., and Shpak, O.V., Unihemispheric slow wave sleep and the state of the

eyes in a white whale,Behavioral Brain Res.

, 129, 125, 2002. With permission.)



12/14

174


CONCLUSIONS

The ultimate question for sleep researchers is the function of REM and non-REM

sleep. Phylogenetic evidence constrains any theory attempting to answer these ques-

tions. We know that sleep amounts vary by more than an order of magnitude across

mammalian species. Either the amount of time spent sleeping has no relation to

underlying function, which would distinguish sleep from many other homeostatically

regulated processes, or sleep need varies considerably across species. The correlates

of this variation should provide some insight into sleep functions.

A survey of the available data indicates that phylogenetic order does not explain

much of the variation of sleep time across species. There is extensive overlap of

both REM and non-REM sleep time between orders, despite the genetic, anatomical,

physiological, and behavioral commonalities within order. Prior data and new data

on primitive mammals and cetaceans indicate a strong negative correlation between

total sleep time and weight. Because metabolic rate is strongly and negativelycorrelated with body mass, this is also a positive correlation between metabolic rate

and sleep time. Some evidence suggests that brain regions with high metabolic rate

have higher levels of sleep deprivation-induced damage. We hypothesized that sleep

serves to repair damage caused by oxidative stress.

38,39

REM sleep amounts are positively correlated with non-REM sleep amounts,

suggesting that REM sleep may work in concert with non-REM sleep. One persistent

hypothesis that has been raised in several forms is that REM sleep serves to stimulate

the brain to prepare for waking after a period of non-REM sleep.

23,40,41

Most of the variation in REM sleep amounts is independent of non-REM sleep

duration. The phylogenetic data indicate that animals born in a relatively immature

state have more REM sleep early in development. One may hypothesize that in these

immature animals REM sleeps activation of the brain facilitates development. In

animals that are more mature at birth, this process may have occurred in utero

andcontinued postnatally in their direct interactions with the environment in waking.

Immature animals are obviously not able to interact with the environment in the

same way. A major mystery that remains is why immaturity at birth should be

correlated with REM sleep time in adulthood.

Marine mammals have sleep patterns that differ greatly from those seen in other

animals. They show unihemispheric sleep, with both hemispheres never being in

deep sleep at the same time. They can sleep while swimming, apparently controlling

muscles bilaterally. Finally, they appear to have little or no REM sleep. Understand-

ing the mechanisms and functional relations underlying these unusual sleep adap-

tations of marine mammals can offer a major insight into the function and mecha-

nisms of sleep.

REFERENCES

1. Siegel, J.M., The evolution of REM sleep, in Lydic, R., Baghdoyan, H.A., Eds.,

Handbook of Behavioral State Control

, CRC Press, Boca Raton, FL, 1999, p. 87.

2. Flanigan, W.F., Sleep and wakefulness in iguanid lizards, Ctenosaura pectinata

, and

Iguana iguana

,Brain Behav. Evol.

, 8, 401, 1973.



13/14


175

3. Huntley, A.C., Electrophysiological and behavioral correlates of sleep in the desert

iguana,Dipsosaurus dorsalis

hallowell, Comp. Biochem. Physiol.

, 86A, 325, 1987.4. Ayala-Guerrero, F., Huitron-Resendiz, S., and Mancilla, R., Characterization of the

raphe nuclei of the reptile Ctenosaura pectinata

, Physiol. Behav.

, 50, 717, 1991.

5. DeVera, L., Gonzalez, J., and Rial, R.V., Reptilean waking EEG: slow waves, spindles,

and evoked potentials,Electroenceph. Clin. Neurophysiol.

, 90, 298, 1994.

6. Flanigan, W.F., Sleep and Wakefulness in Chelonian Reptiles II. The Red-Footed

Tortoise, Gechelone Carbonaria

,Arch. Ital. Biol.

, 112, 253, 1974.

7. Flanigan, W.F., Knight, C., Hartse, and K., Rechtschaffen, A., Sleep and wakefulness

in chelonian reptiles. 1. The box turtle, Terrapene carolina

, Arch. Ital. Biol.

, 112,

227, 1974.

8. Flanigan, W.F., Knight, C.P., Hartse, and K.M., Rechtschaffen, A., Sleep and wake-

fulness in chelonian reptiles I. the box turtle, Terrapene carolina

,Arch. Ital. Biol.

,

112, 227, 1974.

9. Peyrethon, J. and Dusan-Peyrethon, D., Etude polygraphique de cycle veille-sommeil

chez trois genres de reptiles, Seanc. Soc. Biol.

, 162, 181, 1968.10. Shapiro, C.M. and Hepburn, H.R., Sleep in a Schooling Fish, Tilapia, mossambica,

Physiology and Behavior

, 16, 613, 1976.

11. Tobler, I. and Borbely, A.A., Effect of rest deprivation on motor activity of fish,J.

Comp. Physiol. A

., 157, 817, 1985.

12. Shaw, P.J., Tononi, G., Greenspan, R.J., and Robinson, D.F., Stress response genes

protect against lethal effects of sleep deprivation in Drosophila, Nature

, 417, 287,

2002.

13. Shaw, P.J., Cirelli, C., Greenspan, R.J., and Tononi, G., Correlates of sleep and waking

inDrosophila melanogaster

, Science

, 287, 1834, 2000.

14. Hendricks, J.C., Finn, S.M., Panckeri, K.A., Chavkin, J., Williams, J.A., Sehgal, A.,

Pack, A.I., Rest in Drosophila is a sleep-like state, Neuron

, 25, 129, 2000.

15. Zepelin, H., Mammalian sleep, in Kryger, M.H., Roth, T., and Dement, W.C., Eds.,

Principles and Practice of Sleep Medicine

, W.B. Saunders, Philadelphia, 2000, p. 82.

16. Amlaner, C.J. and Ball, N.J., Avian sleep, in Kryger, M.H., Roth, T., Dement, W.C.,Eds., Principles and Practice of Sleep Medicine

, W.B. Saunders Company, Philadel-

phia, 1994, p. 81.

17. Mukhametov, L.M., Supin, A.Y., and Polyakova, I.G., Interhemispheric asymmetry

of the electroencephalographic sleep patterns in dolphins,Brain Res.

, 134, 581, 1977.

18. Schmidt, M.H., Valatx, J.L., Sakai, K., Fort, P., and Jouvet, M., Role of the lateral

preoptic area in sleep-related erectile mechanisms and sleep generation in the rat,J.

Neurosci.

, 20, 6640, 2000.

19. Moore, C.A., Fishman, I.J., and Hirshkowitz, M., Evaluation of erectile dysfunction

and sleep-related erections,J. Psychosom. Res.

, 42, 531, 1997.

20. Affanni, J.M., Cervino, C.O., and Marcos, H.J., Absence of penile erections during

paradoxical sleep, Peculiar penile events during wakefulness and slow wave sleep in

the armadillo,J. Sleep Res.

, 10, 219, 2001.

21. Allison, T. and Cicchetti, D.V., Sleep in mammals: Ecological and constitutional

correlates, Science

, 194, 732, 1976.22. Rechtschaffen, A., Siegel, J.M., Sleep and Dreaming, in Kandel, E.R., Schwartz, J.H.,

and Jessel, T.M., Eds., Principles of Neuroscience

, McGraw Hill, New York, 2000, p. 936.

23. Snyder, F., Toward an evolutionary theory of dreaming,Amer. J. Psychiat.

, 123, 121,

1966.

24. Jouvet-Mounier, D., Astic, L., and Lacote, D., Ontogenesis of the states of sleep in

rat, cat, and guinea pig during the first postnatal month,Dev. Psychobiol.

, 2, 216, 1970.



14/14

176


25. Siegel, J.M., The REM sleep-memory consolidation hypothesis, Science

, 294, 1058,

2001.26. Allison, T., Van Twyver, H., and Goff, W.R., Electrophysiological studies of the

echidna, Tachyglossus aculeatus

, I. Waking and sleep, Arch. Ital. Biol.

, 110, 145,

1972.

27. Allison, T. and Van Twyver, H., Electrophysiological Studies of the Echidna, Tachy-

glossus aculeatus

, II. Dormancy and Hibernation,Arch. Ital. Biol.

, 110, 185, 1972.

28. Siegel, J.M., Manger, P., Nienhuis, R., Fahringer, H.M., and Pettigrew, J., The echidna

Tachyglossus aculeatus combines REM and non-REM aspects in a single sleep state:

implications for the evolution of sleep, J. Neuroscience

, 16, 3500, 1996.

29. Siegel, J.M., Brainstem mechanisms generating REM sleep. In, Kryger, M.H., Roth,

T., Dement, and W.C., Eds., Principles and Practice of Sleep Medicine

, W.B. Saunders

Company, 2000, p. 112.

30. Nicol, S.C., Andersen, N.A., Phillips, N.H., and Berger, R.J., The echidna manifests

typical characteristics of rapid eye movement sleep, Neurosci. Lett. 2000

, Mar. 31;

28, 3 (1): 4952, 283, 49, 2000.31. Siegel, J.M., Manger, P.R., Nienhuis, R., Fahringer, H.M., Shalita, T., and Pettigrew,

J.D., Sleep in the platypus,Neuroscience, 91, 391, 1999.

32. Mukhametov, L.A., Supin, A.Y., and Polyakova, I.G., Interhemispheric asymmetry

of the electroencephalographic sleep patterns in dolphins,Brain Res., 134, 581, 1977.

33. Lyamin, O.I., Mukhametov, L.M., Siegel, J.M., Nazarenko, E.A., Polyakova, I.G.,

and Shpak, O.V., Unihemispheric slow wave sleep and the state of the eyes in a white

whale,Behavioral Brain Res., 129, 125, 2002.

34. Pfurtscheller, G., Neuper, C., and Mohl, W., Event-related desynchronization (ERD)

during visual processing,Int. J. Psychophysiol., 16, 147, 1994.

35. Rattenborg, N.C., Amlaner, C.J., and Lima, S.L., Unilateral eye closure and inter-

hemispheric EEG asymmetry during sleep in the pigeon (Columba livia),Brain Behav.

Evol., 58, 323, 2002.

36. Oleksenko, A.I., Mukhametov, L.M., Polykova, I.G., Supin, A.Y., and Kovalzon, V.M.,

Unihemispheric sleep deprivation in bottlenose dolphins,J. Sleep Res., 1, 40, 1992.37. Eiland, M.M., Lyamin, O.I., and Siegel, J.M., State-related discharge of neurons in

the brainstem of freely moving box turtles, Terrapene carolina major, Arch. Ital.

Biol., 139, 23, 2001.

38. Eiland, M.M., Ramanathan, L., Gulyani, S., Gilliland, M., Bergmann, B.M.,

Rechtschaffen, A., and Siegel, J.M., Increases in amino-cupric-silver staining of the

supraoptic nucleus after sleep deprivation, Brain Res., 945, 1, 2002.

39. Ramanathan, L., Gulyani, S., Nienhuis, R., and Siegel, J.M., Sleep deprivation

decreases superoxide dismutase activity in rat hippocampus and brainstem,Neurore-

port, 13, 1387, 2002.

40. Ephron, H.S. and Carrington, P., Rapid eye movement sleep and cortical homeostasis,

Psychol. Rev.,73, 500, 1966.

41. Vertes, R.P., A life-sustaining function for REM sleep: a theory,Neurosci. Biobehav.

Rev., 10, 371, 1986.


filogenia del sueño

Documents