Timothy C. Roth

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.

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

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.

Variation in memory and the hippocampus across populations from different climates: a common garden approach.

Selection for enhanced cognitive traits is hypothesized to produce enhancements to brain structures that support those traits. Although numerous studies suggest that this pattern is robust, there are several mechanisms that may produce this association. First, cognitive traits and their neural underpinnings may be fixed as a result of differential selection on cognitive function within specific environments. Second, these relationships may be the product of the selection for plasticity, where differences are produced owing to an individuals experiences in the environment. Alternatively, the relationship may be a complex function of experience, genetics and/or epigenetic effects. Using a well-studied model species (black-capped chickadee, Poecile atricapillus), we have for the first time, to our knowledge, addressed these hypotheses. We found that differences in hippocampal (Hp) neuron number, neurogenesis and spatial memory previously observed in wild chickadees persisted in hand-raised birds from the same populations, even when birds were raised in an identical environment. These findings reject the hypothesis that variation in these traits is owing solely to differences in memory-based experiences in different environments. Moreover, neuron number and neurogenesis were strikingly similar between captive-raised and wild birds from the same populations, further supporting the genetic hypothesis. Hp volume, however, did not differ between the captive-raised populations, yet was very different in their wild counterparts, supporting the experience hypothesis. Our results indicate that the production of some Hp factors may be inherited and largely independent of environmental experiences in adult life, regardless of their magnitude, in animals under high selection pressure for memory, while traits such as volume may be more plastic and modified by the environment.

Learning capabilities enhanced in harsh environments: a common garden approach.

Previous studies have suggested that the ability to inhabit harsh environments may be linked to advanced learning traits. However, it is not clear if individuals express such traits as a consequence of experiencing challenging environments or if these traits are inherited. To assess the influence of differential selection pressures on variation in aspects of cognition, we used a common garden approach to examine the response to novelty and problem-solving abilities of two populations of black-capped chickadees (Poecile atricapillus). These populations originated from the latitudinal extremes of the speciess range, where we had previously demonstrated significant differences in memory and brain morphology in a multi-population study. We found that birds from the harsh northern population, where selection for cognitive abilities is expected to be high, significantly outperformed conspecifics from the mild southern population. Our results imply differences in cognitive abilities that may be inherited, as individuals from both populations were raised in and had experienced identical environmental conditions from 10 days of age. Although our data suggest an effect independent of experience, we cannot rule out maternal effects or experiences within the nest prior to day 10 with our design. Nevertheless, our results support the idea that environmental severity may be an important factor in shaping certain aspects of cognition.

A Phylogenetic Analysis of the Correlates of Sleep in Birds

Quantitative comparative studies of sleep have focused exclusively on mammals. Such studies have repeatedly found strong relationships between the time spent in various sleep states and constitutive variables related to morphology, physiology, and life history. These studies influenced the development of several prominent hypotheses for the functions of sleep, but the applicability of these patterns and hypotheses to non‐mammalian taxa is unclear. Here, we present the first quantitative analysis of sleep in a non‐mammalian taxon (birds), focusing on the daily amount of time spent in slow‐wave sleep (SWS) and rapid‐eye movement (REM) sleep as determined by electrophysiological methods. We examined the relationships between constitutive and sleep variables in 23 avian species following earlier studies in mammals, but also considered an index of exposure to predators while asleep and controlled for shared evolutionary history among taxa. Overall, our results were very different from those obtained for mammals. Most remarkably, the relationships between both SWS time and REM sleep time and all constitutive variables were very weak and markedly non‐significant, even though we had adequate power to detect correlations typical of the mammalian data. Only an index of exposure to predation during sleep was significantly related to sleep time, which is the only result common to both birds and mammals. Our results suggest that further insight into the function(s) of sleep across the animal kingdom may require an expansion of sleep research beyond the current mammalian paradigm.

HUNTING BEHAVIOR AND DIET OF COOPER'S HAWKS: AN URBAN VIEW OF THE SMALL-BIRD-IN-WINTER PARADIGM

Abstract We examined the predatory behavior of wintering urban Coopers Hawks (Accipiter cooperii). Eight Coopers Hawks (7 female, 1 male) were radio-tracked intensively during two winter periods from 1999–2001. We observed 179 attacks, 35 of which were successful, for an overall attack success rate of 20%. We recorded an additional 44 kills resulting from unobserved attacks. European Starlings (Sturnus vulgaris), Mourning Doves (Zenaida macroura), and Rock Doves (Columba livia) made up 95% of the prey attacked and 91% of the diet. Smaller birds (<70 g), such as House Sparrows (Passer domesticus), were numerous in the study area but were rarely attacked. Mammals were not included in the diet. Surprise attacks (initiated at close range, often from behind an obstruction), were more successful than “open” attacks, although the latter were more frequent. In addition, attacks on single individuals were significantly more successful than those on flocks. Nonetheless, many attacks were attempted on large flocks. Our results suggest that the smaller bird species (<70 g) in our urban study area were at low risk of predation from Coopers Hawks. Comportamiento de Caza y Dieta de Accipiter cooperii: Una Visión Urbana del Paradigma de Aves Pequeñas durante el Invierno Resumen. Examinamos el comportamiento de depredación de individuos urbanos de la especie Accipiter cooperii durante el período de invernada. Ocho individuos (siete hembras y un macho) fueron seguidos intensamente mediante radio telemetría durante dos períodos invernales desde 1999 hasta 2001. Observamos 179 ataques, de los cuales 35 fueron exitosos, con una tasa general de éxito de ataque del 20%. Adicionalmente, registramos 44 muertes que resultaron de ataques no observados. Sturnus vulgaris, Zenaida macroura y Columba livia compusieron el 95% de las presas atacadas y el 91% de la dieta. Aves pequeñas (<70 g), como Passer domesticus, fueron muy abundantes en el área de estudio pero fueron raramente atacadas. La dieta no incluyó mamíferos. Los ataques sorpresivos (iniciados a una corta distancia, generalmente desde detrás de algún objeto) fueron más exitosos que ataques “abiertos,” aunque estos últimos fueron más frecuentes. Además, los ataques sobre individuos que se encontraban solos fueron significativamente más exitosos que aquellos sobre bandadas. Sin embargo, muchos ataques fueron intentados sobre bandadas grandes. Nuestros resultados sugieren que en nuestra área de estudio urbana las especies de aves más pequeñas (<70 g) tenían un menor riesgo de ser depredadas por A. cooperii.

Ecologically relevant spatial memory use modulates hippocampal neurogenesis

The adult hippocampus in birds and mammals undergoes neurogenesis and the resulting new neurons appear to integrate structurally and functionally into the existing neural architecture. However, the factors underlying the regulation of new neuron production is still under scrutiny. In recent years, the concept that spatial memory affects adult hippocampal neurogenesis has gained acceptance, although results attempting to causally link memory use to neurogenesis remain inconclusive, possibly owing to confounds of motor activity, task difficulty or training for the task. Here, we show that ecologically relevant, spatial memory-based experiences of food caching and retrieving directly affect hippocampal neurogenesis in mountain chickadees (Poecile gambeli). We found that restricting memory experiences in captivity caused significantly lower rates of neurogenesis, as determined by doublecortin expression, compared with captive individuals provided with such experiences. However, neurogenesis rates in both groups of captive birds were still greatly lower than those in free-ranging conspecifics. These findings show that ecologically relevant spatial memory experiences can directly modulate neurogenesis, separate from other confounds that may also independently affect neurogenesis.

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.

Use of Prey Hotspots by an Avian Predator: Purposeful Unpredictability?

The use of space by predators in relation to their prey is a poorly understood aspect of predator‐prey interactions. Classic theory suggests that predators should focus their efforts on areas of abundant prey, that is, prey hotspots, whereas game‐theoretical models of predator and prey movement suggest that the distribution of predators should match that of their prey’s resources. If, however, prey are spatially anchored to one location and these prey have particularly strong antipredator responses that make them difficult to capture with frequent attacks, then predators may be forced to adopt alternative movement strategies to hunt behaviorally responsive prey. We examined the movement patterns of bird‐eating sharp‐shinned hawks (Accipiter striatus) in an attempt to shed light on hotspot use by predators. Our results suggest that these hawks do not focus on prey hotspots such as bird feeders but instead maintain much spatial and temporal unpredictability in their movements. Hawks seldom revisited the same area, and the few frequently used areas were revisited in a manner consistent with unpredictable returns, giving prey little additional information about risk.

Elevation-related differences in memory and the hippocampus in mountain chickadees, Poecile gambeli

Harsh environments may lead to increased demands on memory in animals that rely on memory for survival. We previously showed that winter severity is associated with non-experience-based differences in memory and the hippocampus over a large continental scale in food-caching black-capped chickadees, Poecile atricapillus. However, large climatic differences also occur along steep elevational gradients in montane environments over a small geographical scale. Here, we demonstrate for the first time that large differences in memory and the hippocampus exist over extremely short distances (10 km) along the elevation gradient. We found that food-caching mountain chickadees (P. gambeli) from the highest elevations in the Sierra Nevada Mountains had significantly better spatial memory associated with larger hippocampi, with almost twice the number of hippocampal neurons, than individuals only 600 m lower in elevation. We found similarly large differences in hippocampal neurogenesis rates as indicated by the total number of immature neurons. Our study therefore suggests that climate-related environmental differences can produce dramatic differences in memory and the hippocampus in animals within close proximity on small spatial scales and that currently observed trends in global climate may have significant effects on cognition and the brain.