Hippocampal memory consolidation during sleep: a comparison of mammals and birds

The transition from wakefulness to sleep is marked by pronounced changes in brain activity. The brain rhythms that characterize the two main types of mammalian sleep, slow‐wave sleep (SWS) and rapid eye movement (REM) sleep, are thought to be involved in the functions of sleep. In particular, recent theories suggest that the synchronous slow‐oscillation of neocortical neuronal membrane potentials, the defining feature of SWS, is involved in processing information acquired during wakefulness. According to the Standard Model of memory consolidation, during wakefulness the hippocampus receives input from neocortical regions involved in the initial encoding of an experience and binds this information into a coherent memory trace that is then transferred to the neocortex during SWS where it is stored and integrated within preexisting memory traces. Evidence suggests that this process selectively involves direct connections from the hippocampus to the prefrontal cortex (PFC), a multimodal, high‐order association region implicated in coordinating the storage and recall of remote memories in the neocortex. The slow‐oscillation is thought to orchestrate the transfer of information from the hippocampus by temporally coupling hippocampal sharp‐wave/ripples (SWRs) and thalamocortical spindles. SWRs are synchronous bursts of hippocampal activity, during which waking neuronal firing patterns are reactivated in the hippocampus and neocortex in a coordinated manner. Thalamocortical spindles are brief 7–14 Hz oscillations that may facilitate the encoding of information reactivated during SWRs. By temporally coupling the readout of information from the hippocampus with conditions conducive to encoding in the neocortex, the slow‐oscillation is thought to mediate the transfer of information from the hippocampus to the neocortex. Although several lines of evidence are consistent with this function for mammalian SWS, it is unclear whether SWS serves a similar function in birds, the only taxonomic group other than mammals to exhibit SWS and REM sleep. Based on our review of research on avian sleep, neuroanatomy, and memory, although involved in some forms of memory consolidation, avian sleep does not appear to be involved in transferring hippocampal memories to other brain regions. Despite exhibiting the slow‐oscillation, SWRs and spindles have not been found in birds. Moreover, although birds independently evolved a brain region—the caudolateral nidopallium (NCL)—involved in performing high‐order cognitive functions similar to those performed by the PFC, direct connections between the NCL and hippocampus have not been found in birds, and evidence for the transfer of information from the hippocampus to the NCL or other extra‐hippocampal regions is lacking. Although based on the absence of evidence for various traits, collectively, these findings suggest that unlike mammalian SWS, avian SWS may not be involved in transferring memories from the hippocampus. Furthermore, it suggests that the slow‐oscillation, the defining feature of mammalian and avian SWS, may serve a more general function independent of that related to coordinating the transfer of information from the hippocampus to the PFC in mammals. Given that SWS is homeostatically regulated (a process intimately related to the slow‐oscillation) in mammals and birds, functional hypotheses linked to this process may apply to both taxonomic groups.     

Local sleep homeostasis in the avian brain: convergence of sleep function in mammals and birds?

The function of the brain activity that defines slow wave sleep (SWS) and rapid eye movement (REM) sleep in mammals is unknown. During SWS, the level of electroencephalogram slow wave activity (SWA or 0.5-4.5 Hz power density) increases and decreases as a function of prior time spent awake and asleep, respectively. Such dynamics occur in response to waking brain use, as SWA increases locally in brain regions used more extensively during prior wakefulness. Thus, SWA is thought to reflect homeostatically regulated processes potentially tied to maintaining optimal brain functioning. Interestingly, birds also engage in SWS and REM sleep, a similarity that arose via convergent evolution, as sleeping reptiles and amphibians do not show similar brain activity. Although birds deprived of sleep show global increases in SWA during subsequent sleep, it is unclear whether avian sleep is likewise regulated locally. Here, we provide, to our knowledge, the first electrophysiological evidence for local sleep homeostasis in the avian brain. After staying awake watching David Attenborough's The Life of Birds with only one eye, SWA and the slope of slow waves (a purported marker of synaptic strength) increased only in the hyperpallium--a primary visual processing region--neurologically connected to the stimulated eye. Asymmetries were specific to the hyperpallium, as the non-visual mesopallium showed a symmetric increase in SWA and wave slope. Thus, hypotheses for the function of mammalian SWS that rely on local sleep homeostasis may apply also to birds.     

Sleep and wakefulness in the green iguanid lizard (Iguana iguana)

The reptile Iguana iguana exhibits four states of vigilance: active wakefulness (AW), quiet wakefulness (QW), quiet sleep (QS) and active sleep (AS). Cerebral activity decreases in amplitude and frequency when passing from wakefulness to QS. Both parameters show a slight increase during AS. Heart rate is at a maximum during AW (43.8+/-7.9 beats/min), decreases to a minimum in QS (25.3+/-3.2 beats/min) and increases in AS (36.1+/-5.7 beats/min). Tonical and phasical muscular activity is present in wakefulness, decreases or disappears in QS and reappears in AS. Single or conjugate ocular movements are observed during wakefulness, then disappear in QS and abruptly reappear in AS. Although these reptiles are polyphasic, their sleep shows a tendency to concentrate between 20:00 and 8:00 h. Quiet sleep occupies the greater percentage of the total sleep time. Active sleep episodes are of very short duration, showing an average of 21.5+/-4.9 (mean+/-SD). Compensatory increment of sleep following its total deprivation was significant only for QS. Reaction to stimuli decreased significantly when passing from wakefulness to sleep. It is suggested that the lizard I. iguana displays two sleep phases behaviorally and somatovegetatively similar to slow wave sleep and paradoxical sleep in birds and mammals.     

Sleep in birds: lying on the continuum of activity and rest

Abstract

Sleep is highly organized activity which is associated with decreased muscular activity and reduced response to environmental stimuli. The sleep is regulated by both, circadian and homeostatic mechanisms. Sleep patterns can be studied by behavioral assays by observing different sleep behaviors or by neuronal activity such as EEG (electroencephalogram), EOG (electro-oculogram), and EMG (electromyogram). Sleep is organized into non-rapid eye movement (NREM) and rapid eye movement. The sleep pattern in birds are similar to that in mammals, however, few differences such as existence of unihemispheric sleep (UHS) in almost all birds compared to few marine mammals do exist. The UHS results in asymmetry of the brain function measured as slow wave activity (SWA). Several migrants exhibit sleeplessness and they compensate it by NREM. They employ UHS during their migratory flight to remain alert while sleeping and maintain the balance while flying which is advantageous for these birds. Thus, sleep is of fundamental significance for the animal as it lies on the continuum of activity and rest. The present review focuses on some of above mentioned facts about sleep in higher vertebrates particularly in birds.     

A phylogenetic analysis of sleep architecture in mammals: the integration of anatomy, physiology, and ecology

Among mammalian species, the time spent in the two main "architectural" states of sleep--slow-wave sleep (SWS) and rapid-eye-movement (REM) sleep--varies greatly. Previous comparative studies of sleep architecture found that larger mammals, those with bigger brains, and those with higher absolute basal metabolic rates (BMR) tended to engage in less SWS and REM sleep. Species experiencing a greater risk of predation also exhibited less SWS and REM sleep. In all cases, however, these studies lacked a formal phylogenetic and theoretical framework and used mainly correlational analyses. Using independent contrasts and an updated data set, we extended existing approaches with path analysis to examine the integrated influence of anatomy, physiology, and ecology on sleep architecture. Path model structure was determined by nonmutually exclusive hypotheses for the function of sleep. We found that species with higher relative BMRs engage in less SWS, whereas species with larger relative brain masses engage in more REM sleep. REM sleep was the only sleep variable strongly influenced by predation risk; mammals sleeping in riskier environments engage in less REM sleep. Overall, we found support for some hypotheses for the function of sleep, such as facilitating memory consolidation or learning, but not others, such as energy conservation.     

Behavioral and electrophysiological patterns of wakefulness-sleep states in a lizard.

Four individuals of the lizard Ctenosaura pectinata were chronically implanted for electroencephalographic (EEG), electromyographic (EMG) and electro-oculographic (EOG) recordings. Four different vigilance states were observed throughout the nyctohemeral cycle. These states were: Active wakefulness (Aw), quiet wakefulness (Qw), quiet sleep (Qs) and active sleep (As). Each state displayed its own behavioral and electrophysiological characteristics. EEG waves were similar during Aw and Qw but they diminished in amplitude and frequency when passing from these states to Qs, and both parameters increased during As. Muscular activity was intense in Aw, it decreased during Qw and almost disappeared during Qs. This activity reappeared in a phasic way during As, coinciding with generalized motor manifestations. Ocular activity was intense during Aw but minimal during Qw, it disappeared in Qs and was present intermittently in As. Aw, Qw, Qs and As occupied 5.9%, 25.7%, 67.7% and 0.6% of the 24 hr period, respectively. The frequency and duration of As episodes showed great inter-animal variability and the mean duration was of 12.9 sec. Stimuli reaction threshold was highest during sleep. In conclusion, the lizard Ctenosaura pectinata exhibit two sleep phases (Qs and As) that may be assimilated to slow wave sleep (SWS) and paradoxical sleep (PS) of birds and mammals.     

Asynchronous Eye Closure as an Anti-Predator Behavior in the Western Fence Lizard (Sceloporus occidentalis)

Asynchronous eye closure (ASEC), one eye open while the other is closed, is a behavior observed in birds, some aquatic mammals, and reptiles. In birds and aquatic mammals, ASEC is associated with unihemispheric sleep wherein the cerebral hemisphere contralateral to (i.e. neurologically connected to) the closed eye sleeps while the other cerebral hemisphere remains awake with its associated eye open and functional. Evidence from birds suggests that ASEC is an important anti‐predator adaptation to mediate the trade‐off between the need to remain vigilant and the need to sleep. However, the anti‐predator correlates of ASEC remain largely unstudied in other animals. Here, we present behavioral evidence that ASEC in reptiles is also an anti‐predator adaptation used in response to an increase in the risk of predation. ASEC was measured in captive western fence lizards (Sceloporus occidentalis) individually exposed to three experimental treatments: (1) an empty terrarium, (2) a terrarium housing a novel moving object, and (3) a terrarium housing a live predator (snake). Predator exposure elicited significantly higher levels of vigilance, mostly due to an increase in ASEC. This increase in ASEC came largely at the expense of synchronous eye closure (both eyes closed). Lizards in ASEC also showed a strong tendency to orient their open eye in the direction of the predator. We suggest that lizards engaged in ASEC are sleeping unihemispherically and are thus able to maintain a level of vigilance concurrent with sleep.     

The ontogeny and physiology confirms the dual nature of sleep states

In the Jouvet's laboratory, as early as 1960 the study of the ontogenesis of paradoxical sleep (PS) named "sleep 'with jerks" began in the kitten and led to the first publication in 1961. Then, several species were studied, lamb, rat, human neonates, etc. These works showed that at birth sleep with jerks was preponderant in altricial (immature) species (cat, rat) and the first to appear during the second half of gestation in precocious species (guinea pig). For Jouvet, sleep with jerks is a immature form of PS. Why PS is so important at birth? The maturation of the central nervous system, based on the myelinization, starts in the spinal cord then forwards to the brainstem and forebrain. So, PS mechanisms located in the brainstem are the first to mature and the only one to function. Then the slow wave sleep (SWS) and waking structures become mature. Phylogenetic studies showed that in mammals and birds PS was present even in marsupials and monotremes. Until now only the one exception is the dolphin with a voluntary breathing. To sleep and breath, dolphin has developed an unilateral sleep without classical PS. In other animals, reptiles, amphibians, fishes, PS was not observed with the parameters used in mammals. The study at birth (not yet done) of reptiles would allow perhaps the observation of a temporary PS. Based on these findings, a schematic model of the sleep regulation can be elaborated. Haeckel's aphorism "Ontogeny recapitulates phylogeny" seems true for PS which appears in birds and mammals i.e. at the end of evolution as it appears at the end of gestation when PS cerebral structures are present and mature.     

浙江海岛鸟兽地理生态学的初步研究

对浙江洞头岛及舟山五岛的鸟兽调查表明,海岛动物的种数较相邻大陆为低,但种群密度却高于大陆,岛上的某些种类出现生态位扩展的现象。舟山五岛兽类的种数和岛屿面积呈正相关,其关系式为S=2.12A~(0.29),但种群密度随着岛屿面积的增大而下降。文中据此提出了保护和发展岛屿动物资源的某些措施。     

Electroencephalogram bands modulated by vigilance states in an anuran species: a factor analytic approach

Dramatic changes in neocortical electroencephalogram (EEG) rhythms are associated with the sleep–waking cycle in mammals. Although amphibians are thought to lack a neocortical homologue, changes in rest–activity states occur in these species. In the present study, EEG signals were recorded from the surface of the cerebral hemispheres and midbrain on both sides of the brain in an anuran species, Babina daunchina, using electrodes contacting the meninges in order to measure changes in mean EEG power across behavioral states. Functionally relevant frequency bands were identified using factor analysis. The results indicate that: (1) EEG power was concentrated in four frequency bands during the awake or active state and in three frequency bands during rest; (2) EEG bands in frogs differed substantially from humans, especially in the fast frequency band; (3) bursts similar to mammalian sleep spindles, which occur in non-rapid eye movement mammalian sleep, were observed when frogs were at rest suggesting sleep spindle-like EEG activity appeared prior to the evolution of mammals.     

Weak or strong invaders? A comparison of impact between the native and invaded ranges of mammals and birds alien to Europe

Aim Species introduced to an area outside of their native range are often thought to have higher impact in this new area. We examined whether this is really the case in mammals and birds and to what extent. In particular, we explored how impacts of alien species vary in relationship to invader identity and type of impact. Location Global. Methods We conducted a thorough review of the literature to compare the impact of alien European mammals and birds in their native and invaded ranges. Based on a series of environmental and economic impact scores, we ordered species along a continuum from weak invaders, which have lower impact in the invaded range, to strong invaders, which have higher impact in the invaded range. Results We found that nearly 80% of the mammals are strong invaders, but only half of the birds. Members of these two classes also affect their communities in different ways; birds more often have an impact via hybridization, whereas mammals have stronger impacts via herbivory, transmission of diseases to wildlife and their effects on agriculture, livestock and forestry. Main conclusions Generally, mammals and birds have different impacts when invading new regions. Although there are some bird species that are strong invaders, these remain the exception among birds, whereas most mammals increase their impact in the invaded range. This study provides a deeper insight into patterns of impact in the invaded range.     

Sleep in amphibians and reptiles: a review and a preliminary analysis of evolutionary patterns

Despite the ubiquitous nature of sleep, its functions remain a mystery. In an attempt to address this, many researchers have studied behavioural and electrophysiological phenomena associated with sleep in a diversity of animals. The great majority of vertebrates and invertebrates display a phase of immobility that could be considered as a sort of sleep. Terrestrial mammals and birds, both homeotherms, show two sleep states with distinct behavioural and electrophysiological features. However, whether these features have evolved independently in each clade or were inherited from a common ancestor remains unknown. Unfortunately, amphibians and reptiles, key taxa in understanding the evolution of sleep given their position at the base of the tetrapod and amniote tree, respectively, remain poorly studied in the context of sleep. This review presents an overview of what is known about sleep in amphibians and reptiles and uses the existing data to provide a preliminary analysis of the evolution of behavioural and electrophysiological features of sleep in amphibians and reptiles. We also discuss the problems associated with analysing existing data, as well as the difficulty in inferring homologies of sleep stages based on limited data in the context of an essentially mammalian‐centric definition of sleep. Finally, we highlight the importance of developing comparative approaches to sleep research that may benefit from the great diversity of species with different ecologies and morphologies in order to understand the evolution and functions of sleep.     

Sexual selection and the temporal separation of reproductive events: sperm storage data from reptiles, birds and mammals

The duration of sperm storage by females differs markedly between reptiles (maximum: 2555 d [7 years] and birds (maximum: 117d), with mammals showing both very short (< 1 d) and relatively long periods (maximum: 198 days). The females of many reptiles, probably all birds and some mammals have specialized structures for storing sperm, suggesting that selection for sperm storage has operated on females. Sperm storage, together with delayed implantation and delayed development, separates copulation from fertilization, and hence, copulation from the timing of birth. All three types of separation mechanism occur in mammals. Delayed implantation cannot occur in reptiles and birds because their eggs do not implant, but delayed development occurs in some reptiles. Comparisons among vertebrate classes suggest that sperm storage in the female tract may have an upper limit of a little over 100 days in endotherms: non-hibernating mammals have circumvented this limit by using delayed implantation as an uncoupling mechanism. A long reproductive cycle (up to four years) probably makes sperm storage obligatory for some reptiles. We consider existing hypotheses for prolonged sperm storage and the other reproductive delays, and propose a new hypothesis. Our hypothesis extends Sandell's (1990) hypothesis which states that in mammals delayed implantation has evolved to allow females to time both their copulation and birth seasons optimally. We propose that the other separation mechanisms, namely sperm storage and delayed development, have also evolved for this reason. Sandell suggested that the optimal time for females to copulate is when the opportunities to obtain the best quality male exist, and thus the dislocation of copulation and birth seasons has occurred through sexual selection. We propose that the other two separation mechanisms may also have evolved through sexual selection, in part at least. Of the three separation mechanisms, sperm storage has additional advantages for females in that it also allows them to modify their choice of male after copulation has occurred, through sperm competition. Thus we propose that: (1) all separation mechanisms have evolved when the optimal time for copulation is not compatible with either the optimal time for fertilization (birds) or the optimal time for birth, given a constant gestation period (reptiles, birds and mammals); (2) separation mechanisms have evolved through sexual selection enabling females to improve the quality of the male that fertilizes their eggs, either through pre-copulatory male-male competition (via any of the separation mechanisms) or through post-copulatory sperm competition (via sperm storage).     

Episodic outbreaks of small mammals influence predator community dynamics in an east African savanna ecosystem

Little is known about the dynamics of small mammals in tropical savanna: a critical gap in our understanding of Africa's best known ecosystems. Historical evidence suggested small mammals peak in abundance (outbreak) in Serengeti National Park (SNP), as in agricultural systems. We asked 1) what are bottom–up drivers of small mammals and 2) do predators have top–down effects? We documented dynamics of small mammals, birds of prey, and mammalian carnivores in SNP and agricultural areas. We used climatic fluctuations and differences between unmodified and agricultural systems as perturbations to examine trophic processes, key to understanding responses to climate change and increasing human pressures. Data were derived from intermittent measures of abundance collected 1968–1999, combined with systematic sampling 2000–2010 to construct a 42‐year time series. Data on abundance of black‐shouldered kites (1968–2010), eight other species of rodent‐eating birds (1997–2010), and 10 carnivore species (1993–2010) were also collated. Outbreaks occurred every 3–5 years in SNP, with low or zero abundance between peaks. There was a positive relationship between rainfall in the wet season and 1) small mammal abundance and 2) the probability of an outbreak, both of which increased with negative Southern Oscillation Index values. Rodent‐eating birds and carnivores peaked 6–12 months after small mammals. In agricultural areas, abundance remained higher than in natural habitats. Abundances of birds of prey and mammalian carnivores were extremely low in these areas and not related to small mammal abundance. Small mammals are an important food resource for higher trophic levels in the Serengeti ecosystem. Changes in climate and land use may alter their future dynamics, with cascading consequences for higher trophic levels, including threatened carnivores. Although outbreaks cause substantial damage to crops in agricultural areas, small mammals also play a vital role in maintaining some of the diversity and complexity found in African savanna ecosystems.     

The temporal sequence of the mammalian neocortical neurogenetic program drives mediolateral pattern in the chick pallium

The six-layered neocortex permits complex information processing in all mammalian species. Because its homologous region (the pallium) in nonmammalian amniotes has a different architecture, the ability of neocortical progenitors to generate an orderly sequence of distinct cell types was thought to have arisen in the mammalian lineage. This study, however, shows that layer-specific neuron subtypes do exist in the chick pallium. Deep- and upper-layer neurons are not layered but are segregated in distinct mediolateral domains in vivo. Surprisingly, cultured chick neural progenitors produce multiple layer-specific neuronal subtypes in the same chronological sequence as seen in mammals. These results suggest that the temporal sequence of the neocortical neurogenetic program was already inherent in the last common ancestor of mammals and birds and that mammals use this conserved program to generate a uniformly layered neocortex, whereas birds impose spatial constraints on the sequence to pattern the pallium.     

Genome size and developmental parameters in the homeothermic vertebrates.

Although unrelated to any intuitive notions of organismal complexity, haploid genome sizes (C values) are correlated with a variety of cellular and organismal parameters in different taxa. In some cases, these relationships are universal--notably, genome size correlates positively with cell size in each of the vertebrate classes. Other relationships are apparently relevant only in particular groups. For example, although genome size is inversely correlated with metabolic rate in both mammals and birds, no such relationship is found in amphibians. More recently, it has been suggested that developmental rate and (or) longevity are related to genome size in birds. In the present study, a large dataset was used to examine possible relationships between genome size and various developmental parameters in both birds and mammals. In neither group does development appear to be of relevance to genome size evolution (except perhaps indirectly in birds through the intermediation of body size and (or) within the rodents), a situation very different from that found in amphibians. These findings make it clear that genome size evolution cannot be understood without reference to the particular biology of the organisms under study.     

Pancreatic hormones, insulin/glucagon molar ratios, and somatostatin as determinants of avian carbohydrate metabolism

The endocrine pancreas of birds contains cell populations similar, if not identical, to those found in mammalian pancreata, although the topographical distributions of these cell types differ to some extent. Insulin-secreting (B) cells, glucagon-secreting (A) cells, somatostatin-secreting (D) cells, and pancreatic polypeptide-secreting (PP or F) cells are distributed unequally among the four pancreatic lobes, with most of the A cells located in the third and splenic lobes and PP cells residing in both islet tissue and in acinar tissue. Glucagon appears to be a (the?) major pancreatic hormone involved in metabolic glucoregulation in birds. Yet the essentiality of insulin for this regulatory purpose also has been established. As a result, current thought is directed toward the molar ratio of insulin to glucagon (I/G) as a dominant force in homeostasis rather than toward either of the two hormones separately. Molar I/G ratios have been useful in mammals in studying the needs of the organism to produce glucose to meet a metabolic crisis/need and, when compared with that found in normal Aves, a value of 1.8-2.2 has been established. Such a molar ratio is indicative of a catabolic recovery of nutrients in mammals, suggesting that birds normally are in a catabolic mode (like diabetic, starving, or exercising mammals). Somatostatin (SRIF) is known to inhibit the release of all pancreatic hormones but has a greater inhibitory action on glucagon secretion than it does on any of the other peptides. (It has least effect on APP).(ABSTRACT TRUNCATED AT 250 WORDS)     

The slow isoform of Xenopus troponin I is expressed in developing skeletal muscle but not in the heart

In birds and mammals three isoforms of troponin I (TnI) exist; a slow (TnIs), a fast (TnIf) and a cardiac (TnIc). Although each of these isoforms is expressed in the adult forms of these organisms in a muscle fiber-type-specific manner, the gene encoding TnIs is also expressed within the developing heart of these vertebrates. Herein, our results demonstrate that the developing heart of Xenopus laevis, unlike its counterpart in birds and mammals, does not express the gene encoding the TnIs isoform and that the expression of this gene, as well as the one encoding the Xenopus TnIf isoform, is restricted to skeletal muscle.