The ecological relevance of sleep: the trade-off between sleep, memory and energy conservation

Roth, Timothy C.; Rattenborg, Niels Christian; Pravosudov, Vladimir V.

doi:10.1098/rstb.2009.0209

Cited by 72 publications

(68 citation statements)

References 197 publications

(286 reference statements)

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“…While LTP is one of the most frequently studied aspects of neural plasticity in biomedical studies, its applicability to behavioural ecology has not been fully appreciated but may be of great importance (Brodin 2005b;Roth et al 2010). In the absence of existing studies that focus on LTP in food-hoarding birds, Stewart et al (1999) compared the expression of N-methyl-D-aspartate (NMDA) glutamate receptors in the Hp of hoarding and non-hoarding tits, and found these to be different.…”

Section: Is Hippocampal Volume a Relevant Morphological Measure Of Spmentioning

confidence: 99%

Is bigger always better? A critical appraisal of the use of volumetric analysis in the study of the hippocampus

Roth

Brodin

Smulders

et al. 2010

Phil. Trans. R. Soc. B

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A well-developed spatial memory is important for many animals, but appears especially important for scatter-hoarding species. Consequently, the scatter-hoarding system provides an excellent paradigm in which to study the integrative aspects of memory use within an ecological and evolutionary framework. One of the main tenets of this paradigm is that selection for enhanced spatial memory for cache locations should specialize the brain areas involved in memory. One such brain area is the hippocampus (Hp). Many studies have examined this adaptive specialization hypothesis, typically relating spatial memory to Hp volume. However, it is unclear how the volume of the Hp is related to its function for spatial memory. Thus, the goal of this article is to evaluate volume as a main measurement of the degree of morphological and physiological adaptation of the Hp as it relates to memory. We will briefly review the evidence for the specialization of memory in food-hoarding animals and discuss the philosophy behind volume as the main currency. We will then examine the problems associated with this approach, attempting to understand the advantages and limitations of using volume and discuss alternatives that might yield more specific hypotheses. Overall, there is strong evidence that the Hp is involved in the specialization of spatial memory in scatter-hoarding animals. However, volume may be only a coarse proxy for more relevant and subtle changes in the structure of the brain underlying changes in behaviour. To better understand the nature of this brain/memory relationship, we suggest focusing on more specific and relevant features of the Hp, such as the number or size of neurons, variation in connectivity depending on dendritic and axonal arborization and the number of synapses. These should generate more specific hypotheses derived from a solid theoretical background and should provide a better understanding of both neural mechanisms of memory and their evolution.

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Section: Is Hippocampal Volume a Relevant Morphological Measure Of Spmentioning

confidence: 99%

Is bigger always better? A critical appraisal of the use of volumetric analysis in the study of the hippocampus

Roth

Brodin

Smulders

et al. 2010

Phil. Trans. R. Soc. B

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“…Biomedical researchers have focused on the relationship between sleep and memory for quite a while, but debates continue on whether and/or how sleep might affect memory and neurobiological processes in the brain. Roth et al (2010b) provide a review of research on the relationship between sleep, memory and the brain and argue that the food-caching paradigm may present a great model to advance our understanding of such a relationship. No research to date has investigated sleep in food-caching animals, and taking advantage of the food-caching system may provide novel insights into the role of sleep in memory consolidation.…”

Section: Mechanisms Underlying Hippocampal Memory Processingmentioning

confidence: 99%

Integrating ecology, psychology and neurobiology within a food-hoarding paradigm

Pravosudov

Smulders

2010

Phil. Trans. R. Soc. B

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Many animals regularly hoard food for future use, which appears to be an important adaptation to a seasonally and/or unpredictably changing environment. This food-hoarding paradigm is an excellent example of a natural system that has broadly influenced both theoretical and empirical work in the field of biology. The food-hoarding paradigm has played a major role in the conceptual framework of numerous fields from ecology (e.g. plant -animal interactions) and evolution (e.g. the coevolution of caching, spatial memory and the hippocampus) to psychology (e.g. memory and cognition) and neurobiology (e.g. neurogenesis and the neurobiology of learning and memory). Many food-hoarding animals retrieve caches by using spatial memory. This memory-based behavioural system has the inherent advantage of being tractable for study in both the field and laboratory and has been shaped by natural selection, which produces variation with strong fitness consequences in a variety of taxa. Thus, food hoarding is an excellent model for a highly integrative approach to understanding numerous questions across a variety of disciplines. Recently, there has been a surge of interest in the complexity of animal cognition such as future planning and episodic-like-memory as well as in the relationship between memory, the environment and the brain. In addition, new breakthroughs in neurobiology have enhanced our ability to address the mechanisms underlying these behaviours. Consequently, the field is necessarily becoming more integrative by assessing behavioural questions in the context of natural ecological systems and by addressing mechanisms through neurobiology and psychology, but, importantly, within an evolutionary and ecological framework. In this issue, we aim to bring together a series of papers providing a modern synthesis of ecology, psychology, physiology and neurobiology and identifying new directions and developments in the use of food-hoarding animals as a model system.

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Section: Research Articlementioning

confidence: 99%

“…Skin temperature was measured every 5 min. We compared the duration of time during which the bats had a T skin above 30°C, because higher brain temperature favours the possibility of sleeping and memory consolidation (Palchykova et al, 2002;Roth et al, 2010). We used differences in the time spent with T skin >30°C as an indicator of the possibility of potential memory consolidation.…”

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confidence: 99%

“…is normally formed after repeated learning events (Smid et al, 2007) and sleep enhances this process (Palchykova et al, 2002;Roth et al, 2010). Sleep deprivation has negative effects on both memory consolidation [the storage of initial memory representations into long-term memory by stabilization, enhancement and integration processes (Stickgold, 2005)] and retention (Graves et al, 2003;Guan et al, 2004).Recently, an interesting conflict between energy conservation and sleep was discovered in hibernation and torpor using mammals (for review, see Roth et al, 2010). Such mammals are able to decrease their body temperature to save energy during periods of food deficiency (Geiser, 2008).…”

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confidence: 99%

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Do greater mouse-eared bats experience a trade-off between energy conservation and learning?

Ruczyński

Clarin

Siemers

2014

Journal of Experimental Biology

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Bats, some species of rodents and some birds are able to save energy during the summer period by decreasing their body temperature and falling into torpor. Some studies indicate that torpor prevents sleeping and causes effects similar to sleep deprivation. Impairment of processes stabilizing memory slows down learning accuracy and speed. We conducted two experiments to test whether greater mouse-eared bats, Myotis myotis, which commonly use torpor during the summer period, experience a trade-off between energy savings and learning abilities. We compared learning speed and accuracy in bats that were exposed to low (7°C) and higher ambient temperatures (22°C) between training and experimental sessions. Tests were conducted in experiments with food reward (food search) and without food reward (perch search). Time spent with the skin temperature above 30°C was significantly longer for bats exposed to 22°C than for those exposed to 7°C, and longer in experiments with food reward than without food reward. We observed only a very weak tendency for better accuracy and shorter search times in bats exposed to 22°C than in those exposed to 7°C. Our data indicate that memory consolidation of bats under natural conditions is not affected by daily torpor when bats are in good condition and may therefore defend against a rapid fall into torpor. We suggest that homeostatic processes connected with the circadian rhythm allow protection of the consolidation of memory for relatively simple tasks despite time spent in torpor. KEY WORDS: Life history, Memory consolidation, Memory retention, Normothermy, Torpor INTRODUCTIONLong-term memory is important for many animals in a variety of different contexts (Roth et al., 2010). Good memory allows for quick and effective rediscovering of food resources and hides, identification of conspecifics, etc. (Shettleworth, 2001;Stoddard et al., 1991). Storage of accurate memories is an active and costly process involving maintenance and repair of neural structures (Dukas, 1999). Therefore, animals may experience conflicts between the benefits and costs of memory retention (the keeping of memory over prolonged periods of time) (Chancellor et al., 2011;Roth and Pravosudov, 2009); for example, food-catching birds living in harsh climates have developed a larger hippocampus volume than those from milder areas, which may result in enhanced spatial memory and better survival in birds from harsh climates. A memory RESEARCH ARTICLE1 Sensory Ecology Group, Max Planck Institute for Ornithology, Eberhard-GwinnerStraße 11, 82319 Seewiesen, Germany. is normally formed after repeated learning events (Smid et al., 2007) and sleep enhances this process (Palchykova et al., 2002;Roth et al., 2010). Sleep deprivation has negative effects on both memory consolidation [the storage of initial memory representations into long-term memory by stabilization, enhancement and integration processes (Stickgold, 2005)] and retention (Graves et al., 2003;Guan et al., 2004).Recently, an interesting conflict between energ...

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The ecological relevance of sleep: the trade-off between sleep, memory and energy conservation

Cited by 72 publications

References 197 publications

Is bigger always better? A critical appraisal of the use of volumetric analysis in the study of the hippocampus

Is bigger always better? A critical appraisal of the use of volumetric analysis in the study of the hippocampus

Integrating ecology, psychology and neurobiology within a food-hoarding paradigm

Do greater mouse-eared bats experience a trade-off between energy conservation and learning?

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