Dolores Martinez-Gonzalez

Avian sleep homeostasis: Convergent evolution of complex brains, cognition and sleep functions in mammals and birds

Birds are the only taxonomic group other than mammals that exhibit high-amplitude slow-waves in the electroencephalogram (EEG) during sleep. This defining feature of slow-wave sleep (SWS) apparently evolved independently in mammals and birds, as reptiles do not exhibit similar EEG activity during sleep. In mammals, the level of slow-wave activity (SWA) (low-frequency spectral power density) during SWS increases and decreases as a function of prior time spent awake and asleep, respectively, and therefore reflects homeostatically regulated sleep processes potentially tied to the function of SWS. Although birds also exhibit SWS, previous sleep deprivation studies in birds did not detect a compensatory increase in SWS-related SWA during recovery, as observed in similarly sleep-deprived mammals. This suggested that, unlike mammalian SWS, avian SWS is not homeostatically regulated, and therefore might serve a different function. However, we recently demonstrated that SWA during SWS increases in pigeons following short-term sleep deprivation. Herein we summarize research on avian sleep homeostasis, and cast our evidence for this phenomenon within the context of theories for the function of SWS in mammals. We propose that the convergent evolution of homeostatically regulated SWS in mammals and birds was directly linked to the convergent evolution of large, heavily interconnected brains capable of performing complex cognitive processes in each group. Specifically, as has been proposed for mammals, the interconnectivity that forms the basis of complex cognition in birds may also instantiate slow, synchronous network oscillations during SWS that in turn maintain interconnectivity and cognition at an optimal level.

Increased EEG spectral power density during sleep following short‐term sleep deprivation in pigeons (Columba livia): evidence for avian sleep homeostasis

Birds provide a unique opportunity to evaluate current theories for the function of sleep. Like mammalian sleep, avian sleep is composed of two states, slow‐wave sleep (SWS) and rapid eye‐movement (REM) sleep that apparently evolved independently in mammals and birds. Despite this resemblance, however, it has been unclear whether avian SWS shows a compensatory response to sleep loss (i.e., homeostatic regulation), a fundamental aspect of mammalian sleep potentially linked to the function of SWS. Here, we prevented pigeons (Columba livia) from taking their normal naps during the last 8 h of the day. Although time spent in SWS did not change significantly following short‐term sleep deprivation, electroencephalogram (EEG) slow‐wave activity (SWA; i.e., 0.78–2.34 Hz power density) during SWS increased significantly during the first 3 h of the recovery night when compared with the undisturbed night, and progressively declined thereafter in a manner comparable to that observed in similarly sleep‐deprived mammals. SWA was also elevated during REM sleep on the recovery night, a response that might reflect increased SWS pressure and the concomitant ‘spill‐over’ of SWS‐related EEG activity into short episodes of REM sleep. As in rodents, power density during SWS also increased in higher frequencies (9–25 Hz) in response to short‐term sleep deprivation. Finally, time spent in REM sleep increased following sleep deprivation. The mammalian‐like increase in EEG spectral power density across both low and high frequencies, and the increase in time spent in REM sleep following sleep deprivation suggest that some aspects of avian and mammalian sleep are regulated in a similar manner.

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 Attenboroughs 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.

Predator-induced plasticity in sleep architecture in wild-caught Norway rats (Rattus norvegicus)

Sleep is a prominent behaviour in the lives of animals, but the unresponsiveness that characterizes sleep makes it dangerous. Mammalian sleep is composed of two neurophysiological states: slow wave sleep (SWS) and rapid-eye-movement (REM) sleep. Given that the intensity of stimuli required to induce an arousal to wakefulness is highest during deep SWS or REM sleep, mammals may be most vulnerable during these states. If true, then animals should selectively reduce deep SWS and REM sleep following an increase in the risk of predation. To test this prediction, we simulated a predatory encounter with 10 wild-caught Norway rats (Rattus norvegicus), which are perhaps more likely to exhibit natural anti-predator responses than laboratory strains. Immediately following the encounter, rats spent more time awake and less time in SWS and REM sleep. The reduction of SWS was due to the shorter duration of SWS episodes, whereas the reduction of REM sleep was due to a lower number of REM sleep episodes. The onset of SWS and REM sleep was delayed post-encounter by about 20 and 100 min, respectively. The reduction of REM sleep was disproportionately large during the first quarter of the sleep phase, and slow wave activity (SWA) (0.5-4.5 Hz power density) was lower during the first 10 min of SWS post-encounter. An increase in SWA and REM sleep was observed later in the sleep phase, which may reflect sleep homeostasis. These results suggest that aspects of sleep architecture can be adjusted to the prevailing risk of predation.

Ecology and Neurophysiology of Sleep in Two Wild Sloth Species

STUDY OBJECTIVES Interspecific variation in sleep measured in captivity correlates with various physiological and environmental factors, including estimates of predation risk in the wild. However, it remains unclear whether prior comparative studies have been confounded by the captive recording environment. Herein we examine the effect of predation pressure on sleep in sloths living in the wild. DESIGN Comparison of two closely related sloth species, one exposed to predation and one free from predation. SETTING Panamanian mainland rainforest (predators present) and island mangrove (predators absent). PARTICIPANTS Mainland (Bradypus variegatus, five males and four females) and island (Bradypus pygmaeus, six males) sloths. INTERVENTIONS None. MEASUREMENTS AND RESULTS Electroencephalographic (EEG) and electromyographic (EMG) activity was recorded using a miniature data logger. Although both species spent between 9 and 10 h per day sleeping, the mainland sloths showed a preference for sleeping at night, whereas island sloths showed no preference for sleeping during the day or night. Standardized EEG activity during nonrapid eye movement (NREM) sleep showed lower low-frequency power, and increased spindle and higher frequency power in island sloths when compared to mainland sloths. CONCLUSIONS In sloths sleeping in the wild, predation pressure influenced the timing of sleep, but not the amount of time spent asleep. The preference for sleeping at night in mainland sloths may be a strategy to avoid detection by nocturnal cats. The pronounced differences in the NREM sleep EEG spectrum remain unexplained, but might be related to genetic or environmental factors.

Avian Versus Mammalian Sleep: the Fruits of Comparing Apples and Oranges

Insight into the functions of sleep in humans can be gained through studying sleep in animals. In contrast to model-based approaches which emphasize similarities between sleep in humans and animals amenable to experimental manipulation, comparative-based approaches give equal emphasis to the similarities and differences in sleep across the animal kingdom, and thereby aim to reveal overarching principles not readily apparent using other approaches. Avian sleep serves as a prime example. Birds independently evolved rapid eye movement (REM) and non-REM sleep, states that are in many, but, importantly, not all respects comparable to those in mammals. When compared to the sleep traits specific to one group, those shared by mammals and birds are more likely to be involved in fundamental functions. In this review, we summarize recent advances in our understanding of avian sleep, and the implications that such comparative work has for understanding sleep in mammals, including ourselves.

Episodic-like memory and divergent brain systems in mammals and birds.

In their review in PNAS, Allen and Fortin use a comparative neuroanatomical approach to gain insight into the evolution of episodic memory (1). The authors suggest that, as in humans, episodic-like memory in nonhuman mammals depends on a system consisting of the hippocampus, parahippocampal region, and prefrontal cortex (PFC), and, in birds, a similar system consisting of the hippocampus, area parahippocampalis, and nidopallium caudolaterale (NCL), the avian analog of the PFC. Although we agree that the behavioral evidence for episodic-like memory in birds is compelling, in contrast to Allen and Fortin, our interpretation of the available neuroanatomical evidence indicates that key components of this system are missing in birds. In mammals, the PFC is thought to assess the relevance of episodic memories recalled from the hippocampus via its connections with the hippocampus, parahippocampal region, and other higher association areas reactivated during recall and to, then, orchestrate behavior accordingly through projections to motor areas (1). Like the PFC, the NCL is reciprocally connected to higher association and motor output regions and appears to perform executive functions (2). However, of the laboratories (at least four) that have addressed this question, none has detected connections between the NCL and the area parahippocampalis or hippocampus (3) (reviewed in ref. 4). This may be related to the fact that the PFC and NCL are analogous structures that evolved independently and develop from different parts of the pallium; in mammals, the PFC develops from the dorsal pallium, whereas in birds the NCL and the rest of the dorsal ventricular ridge (DVR) develop from the lateral and ventral pallium (5). Interestingly, in birds, rather than developing into a higher-order multimodal association area, such as the PFC, the dorsal pallium develops into the hyperpallium, a structure composed of primary visual and somatosensory/motor subregions (5). Nonetheless, consistent with its developmental homology with mammalian dorsal pallial derivatives, the hyperpallium shares PFC-like connections to the hippocampus, area parahippocampalis, and motor output regions (5) and, as suggested by Bingman and coworkers, may bridge the apparent gap between the hippocampus and NCL by conveying spatial (visual and olfactory) information via known projections to the NCL (3). The NCL could then integrate this information with that received from other association regions in the DVR and, thereby, orchestrate adaptive behaviors. Although this pathway may provide a route for integrating information processed by the hippocampus, hyperpallium, and DVR, additional differences exist between birds and mammals that likely influence the nature of episodic-like memory in the two groups. Unlike mammals, wherein highly processed information from virtually the entire neocortex converges in the hippocampus, enabling it to serve as a node for rapidly encoding experiences and initiating their recall, the avian hippocampus only receives olfactory and visual input and is not privy to much of the information processed by association regions in the DVR (nidopallium and mesopallium), in addition to the NCL (4). Given these fundamental differences in neuroanatomy, to the extent that episodic-like memory depends on information reaching the hippocampus, such memories may be qualitatively different between birds and mammals.

Activation of state-regulating neurochemical systems in newborn and embryonic chicks

Coordinated activity in different sets of widely-projecting neurochemical systems characterize waking (W) and sleep (S). How and when this coordination is achieved during development is not known. We used embryos and newborns of a precocial bird species (chickens) to assess developmental activation in different neurochemical systems using cFos expression, which has been extensively employed to examine cellular activation during S and W in adult mammals. Similarly to adult mammals, newborn awake chicks showed significantly higher cFos expression in W-active hypocretin/orexin (H/O), serotonergic Dorsal Raphe, noradrenergic Locus Coeruleus and cholinergic Laterodorsal and Pedunculopontine Tegmental (Ch-LDT/PT) neurons when compared to sleeping chicks. cFos expression was significantly correlated both between these systems, and with the amount of W. S-active melanin-concentrating hormone (MCH) neurons showed very low cFos expression with no difference between sleeping and awake chicks, possibly due to the very short duration of S episodes. In embryonic chicks, cFos expression was low or absent across all five systems at embryonic day (E) 12. Unexpectedly, a strong activation was seen at E16 in H/O neurons. The highest activation of Ch-LDT/PT (also S-active) and MCH neurons was seen at E20. These data suggest that maturation of arousal systems is achieved soon after hatching, while S-control networks are active in late chick embryos.

A bird's eye view of sleep

In the News Focus story “Simple sleepers” (18 July, p. [334][1]), E. Youngsteadt highlights recent advances, derived from genetic research in fruit flies and other “simple” animal models, in our understanding of sleep. The power of this genetic approach is undeniable, but the simplicity that