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N C Rattenborg

Publications and source records attributed to N C Rattenborg.

3 recordsLinked to original sources

Unilateral eye closure and interhemispheric EEG asymmetry during sleep in the pigeon (Columba livia).

Aquatic mammals (i.e., Cetaceans, eared seals and manatees) and birds show interhemispheric asymmetries (IA) in slow-wave sleep-related electroencephalographic (EEG) activity, suggesting that the depth of sleep differs between hemispheres. In birds, an association between unilateral eye closure and IA has been reported in five species from three orders (i.e., Galliformes, Charadriiformes, and Anseriformes). Moreover, unilateral eye closure has been observed during behaviorally defined sleep in 29 species from 13 avian orders, suggesting that birds in general display IA during sleep. Despite the apparent prevalence of unilateral eye closure and IA in birds, previous work did not detect IA in the pigeon, thereby challenging the conclusion that this is a general feature of birds. Using digital period amplitude analysis, an objective method for quantifying EEG power (a measure of wave amplitude) across different frequencies, we demonstrate that pigeons do, in fact, display an association between unilateral eye closure and IA. For a given hemisphere, standardized 2-4 Hz EEG power was greater when the contralateral eye was closed when compared to open. We also found that pigeons used the open eye during IA to monitor their environment. In addition, individual pigeons showed a bias for keeping one eye open more than the other. The direction (left vs. right) of this bias differed across birds, and appeared to be influenced by the structure of the surrounding environment. Finally, with the addition of pigeons (order Columbiformes), IA associated with unilateral eye closure has been recorded in four avian orders, suggesting that this form of sleep is widespread in birds.

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Behavioral, neurophysiological and evolutionary perspectives on unihemispheric sleep.

Several animals mitigate the fundamental conflict between sleep and wakefulness by engaging in unihemispheric sleep, a unique state during which one cerebral hemisphere sleeps while the other remains awake. Among mammals, unihemispheric sleep is restricted to aquatic species (Cetaceans, eared seals and manatees). In contrast to mammals, unihemispheric sleep is widespread in birds, and may even occur in reptiles. Unihemispheric sleep allows surfacing to breathe in aquatic mammals and predator detection in birds. Despite the apparent utility in being able to sleep unihemispherically, very few mammals sleep in this manner. This is particularly interesting since the reptilian ancestors to mammals may have slept unihemispherically. The relative absence of unihemispheric sleep in mammals suggests that a trade off exists between unihemispheric sleep and other adaptive brain functions occurring during sleep or wakefulness. Presumably, the benefits of sleeping unihemispherically only outweigh the costs under extreme circumstances such as sleeping at sea. Ultimately, a greater understanding of the reasons for little unihemispheric sleep in mammals promises to provide insight into the functions of sleep, in general.

Animals↗

Facultative control of avian unihemispheric sleep under the risk of predation.

Birds and aquatic mammals are the only taxonomic groups known to exhibit unihemispheric slow-wave sleep (USWS). In aquatic mammals, USWS permits sleep and breathing to occur concurrently in water. However, the function of avian USWS has been unclear. Our study is based on the premise that avian USWS serves a predator detection function, since the eye contralateral to the awake hemisphere remains open during USWS. If USWS functions as a form of predator detection, then birds should be able to control both the proportion of slow-wave sleep composed of USWS and the orientation of the open eye in response to changes in predation risk. To test these predictions we recorded eye state and the EEG of mallard ducks (Anas platyrhynchos) sleeping in groups of four birds arranged in a row. Birds at the ends of the row were more exposed than those in the central positions, who were flanked on both sides by other birds, and thus should perceive a greater risk of predation. Consistent with a predator detection function, when compared to birds in the group's center, birds at the exposed ends of the row showed a 150% increase in USWS and a preference for directing the open eye away from the group, the direction from which a predator is most likely to approach. Furthermore, during USWS mallards responded rapidly to threatening visual stimuli presented to the open eye. This ability to facultatively control sleep and wakefulness simultaneously in different regions of the brain probably involves the neuroanatomical interhemispheric separation responsible for independent hemispheric functioning during wakefulness in birds.

Animals↗