Biomedical subjects

N S Clayton

Publications and source records attributed to N S Clayton.

At least 19 recordsLinked to original sources

PubMed2002

Changes in spatial memory mediated by experimental variation in food supply do not affect hippocampal anatomy in mountain chickadees (Poecile gambeli).

Earlier reports suggested that seasonal variation in food-caching behavior (caching intensity and cache retrieval accuracy) might correlate with morphological changes in the hippocampal formation, a brain structure thought to play a role in remembering cache locations. We demonstrated that changes in cache retrieval accuracy can also be triggered by experimental variation in food supply: captive mountain chickadees (Poecile gambeli) maintained on limited and unpredictable food supply were more accurate at recovering their caches and performed better on spatial memory tests than birds maintained on ad libitum food. In this study, we investigated whether these two treatment groups also differed in the volume and neuron number of the hippocampal formation. If variation in memory for food caches correlates with hippocampal size, then our birds with enhanced cache recovery and spatial memory performance should have larger hippocampal volumes and total neuron numbers. Contrary to this prediction we found no significant differences in volume or total neuron number of the hippocampal formation between the two treatment groups. Our results therefore indicate that changes in food-caching behavior and spatial memory performance, as mediated by experimental variations in food supply, are not necessarily accompanied by morphological changes in volume or neuron number of the hippocampal formation in fully developed, experienced food-caching birds.

Animals↗

PubMed2001

Effects of experience and social context on prospective caching strategies by scrub jays.

Social life has costs associated with competition for resources such as food. Food storing may reduce this competition as the food can be collected quickly and hidden elsewhere; however, it is a risky strategy because caches can be pilfered by others. Scrub jays (Aphelocoma coerulescens) remember 'what', 'where' and 'when' they cached. Like other corvids, they remember where conspecifics have cached, pilfering them when given the opportunity, but may also adjust their own caching strategies to minimize potential pilfering. To test this, jays were allowed to cache either in private (when the other bird's view was obscured) or while a conspecific was watching, and then recover their caches in private. Here we show that jays with prior experience of pilfering another bird's caches subsequently re-cached food in new cache sites during recovery trials, but only when they had been observed caching. Jays without pilfering experience did not, even though they had observed other jays caching. Our results suggest that jays relate information about their previous experience as a pilferer to the possibility of future stealing by another bird, and modify their caching strategy accordingly.

Animals↗

PubMed2001

Elements of episodic-like memory in animals.

A number of psychologists have suggested that episodic memory is a uniquely human phenomenon and, until recently, there was little evidence that animals could recall a unique past experience and respond appropriately. Experiments on food-caching memory in scrub jays question this assumption. On the basis of a single caching episode, scrub jays can remember when and where they cached a variety of foods that differ in the rate at which they degrade, in a way that is inexplicable by relative familiarity. They can update their memory of the contents of a cache depending on whether or not they have emptied the cache site, and can also remember where another bird has hidden caches, suggesting that they encode rich representations of the caching event. They make temporal generalizations about when perishable items should degrade and also remember the relative time since caching when the same food is cached in distinct sites at different times. These results show that jays form integrated memories for the location, content and time of caching. This memory capability fulfils Tulving's behavioural criteria for episodic memory and is thus termed 'episodic-like'. We suggest that several features of episodic memory may not be unique to humans.

Animals↗

PubMed2001

Hippocampal volume does not change seasonally in a non food-storing songbird.

Seasonal differences in hippocampal morphology have been reported in food-storing birds. Non food-storing species have not been investigated however. It is therefore unclear whether seasonal changes in the hippocampus are specifically related to food-storing or reflect a more general seasonal mechanism that occurs in both food-storing and non food-storing birds alike. We determined the volumes of the hippocampal formation and remaining telencephalon in the non-storing male song sparrow (Melospiza melodies morphna) in two experiments comparing birds collected in the spring and fall of 1992-94 (Experiment 1) and 1997 (Experiment 2). Although pronounced seasonal changes in song control nuclei such as the HVC and RA were previously reported for the same brains used in Experiment 1, we found that hippocampal volume did not change with season in either Experiment 1 or 2 for these song sparrow brains. These results suggest that seasonal changes in the hippocampus do not occur in this non food-storing species and may be specific to food-storing birds.

Animals↗

PubMed2001

Effects of demanding foraging conditions on cache retrival accuracy in food-caching mountain chickadees (Poecile gambeli).

Birds rely, at least in part, on spatial memory for recovering previously hidden caches but accurate cache recovery may be more critical for birds that forage in harsh conditions where the food supply is limited and unpredictable. Failure to find caches in these conditions may potentially result in death from starvation. In order to test this hypothesis we compared the cache recovery behaviour of 24 wild-caught mountain chickadees (Poecile gambeli), half of which were maintained on a limited and unpredictable food supply while the rest were maintained on an ad libitum food supply for 60 days. We then tested their cache retrieval accuracy by allowing birds from both groups to cache seeds in the experimental room and recover them 5 hours later. Our results showed that birds maintained on a limited and unpredictable food supply made significantly fewer visits to non-cache sites when recovering their caches compared to birds maintained on ad libitum food. We found the same difference in performance in two versions of a one-trial associative learning task in which the birds had to rely on memory to find previously encountered hidden food. In a non-spatial memory version of the task, in which the baited feeder was clearly marked, there were no significant differences between the two groups. We therefore concluded that the two groups differed in their efficiency at cache retrieval. We suggest that this difference is more likely to be attributable to a difference in memory (encoding or recall) than to a difference in their motivation to search for hidden food, although the possibility of some motivational differences still exists. Overall, our results suggest that demanding foraging conditions favour more accurate cache retrieval in food-caching birds.

Animals↗

PubMed2001

Long-term unpredictable foraging conditions and physiological stress response in mountain chickadees (Poecile gambeli).

Birds respond to short-term deterioration in foraging conditions by increasing their plasma level of corticosterone but the physiological effects of long-term deterioration in food supplies are not well known. In resident passerine birds that winter in temperate climates, such as the mountain chickadee (Poecile gambeli), the food supply may be limited and unpredictable over long periods of time. Whether the long-term limited and unpredictable food supply has an effect on (a) baseline levels of corticosterone and (b) the adrenocortical stress response to a standardized acute stress of handling and restraint in mountain chickadees was assessed. For a period of 94 days, one group of chickadees was maintained on limited and unpredictable food (food-restricted) and the other group was maintained on an ad libitum food supply. The food-restricted birds had significantly higher baseline levels of corticosterone than those maintained on ad libitum food. All birds responded to the acute stressor by an increasing secretion of corticosterone but there were no differences between the treatment groups in their stress response. There was a significant effect of sex on the stress response, with females reaching higher levels of corticosterone and responding at a faster rate than males. These results suggest that permanent resident birds wintering in harsh environments may have elevated levels of corticosterone on a long-term basis. Whereas other factors, such as day length and ambient temperature, may contribute to energetic hardship during the winter, the results showed that limited and unpredictable food alone can trigger significant changes in baseline levels of plasma corticosterone. The potential costs and benefits of long-term increased corticosterone levels in resident food-caching birds are discussed.

Adrenal Cortex↗

PubMed2001

Testing episodic memory in animals: a new approach.

Episodic memory involves the encoding and storage of memories concerned with unique personal experiences and their subsequent recall, and it has long been the subject of intensive investigation in humans. According to Tulving's classical definition, episodic memory "receives and stores information about temporally dated episodes or events and temporal-spatial relations among these events." Thus, episodic memory provides information about the 'what' and 'when' of events ('temporally dated experiences') and about 'where' they happened ('temporal-spatial relations'). The storage and subsequent recall of this episodic information was thought to be beyond the memory capabilities of nonhuman animals. Although there are many laboratory procedures for investigating memory for discrete past episodes, until recently there were no previous studies that fully satisfied the criteria of Tulving's definition: they can all be explained in much simpler terms than episodic memory. However, current studies of memory for cache sites in food-storing jays provide an ethologically valid model for testing episodic-like memory in animals, thereby bridging the gap between human and animal studies memory. There is now a pressing need to adapt these experimental tests of episodic memory for other animals. Given the potential power of transgenic and knock-out procedures for investigating the genetic and molecular bases of learning and memory in laboratory rodents, not to mention the wealth of knowledge about the neuroanatomy and neurophysiology of the rodent hippocampus (a brain area heavily implicated in episodic memory), an obvious next step is to develop a rodent model of episodic-like memory based on the food-storing bird paradigm. The development of a rodent model system could make an important contribution to our understanding of the neural, molecular, and behavioral mechanisms of mammalian episodic memory.

Animals↗

PubMed2001

Hippocampal growth and maintenance depend on food-caching experience in juvenile mountain chickadees (Poecile gambeli).

This experiment investigated the development of caching behavior and the hippocampus (HF) in postfledging mountain chickadees (Poecile gambeli). From Days 35 to 53, the number of seeds stored increased but the proportion recovered did not. Birds that stored and recovered during 3 or more trials had significantly enlarged HF but not telencephalon volumes (experienced) compared with those that stored but did not recover (store only) and those deprived of caching experience altogether (deprived). HF size did not increase linearly with the number of experience trials. Birds that received less than 3 experience trials did not differ from deprived birds in HF size, suggesting a threshold effect. Experienced birds prevented from caching for 1 month had significantly smaller HF volumes than those examined immediately after caching experience and did not differ from deprived birds. Experience of both storing and recovery is required to initiate growth and maintain HF size.

Animals↗

PubMed2001

Scrub jays (Aphelocoma coerulescens) form integrated memories of the multiple features of caching episodes.

Four experiments examined whether food-storing scrub jays remember when and where they cached different foods. The scrub jays cached and recovered perishable and nonperishable foods in visuospatially distinct and trial-unique cache sites. They rapidly learned to avoid searching for foods that had perished by the time of recovery, while continuing to search for the same foods after shorter retention intervals when the foods were still fresh. The temporal control of searching at recovery was also observed when the familiarity of cache sites did not provide any information about the time of caching and when the same food was cached in distinct sites at different times. The authors argue that the jays formed an integrated memory for the location and time of caching of particular foods.

Animals↗

PubMed2000

Rapid effects of corticosterone on cache recovery in mountain chickadees (Parus gambeli).

Environmental perturbations increase adrenal activity in several vertebrates. Increases in corticosterone may serve as a proximate trigger whereby organisms can rapidly adapt their behavior to survive environmental fluctuations. In food-caching songbirds, inclement weather may present the need to alter caching and/or retrieval behaviors to ensure food supplies. We hypothesized that corticosterone may increase the rate of caching and/or retrieval behaviors in the mountain chickadee, a food-storing songbird, and tested if these potential effects were mediated by alterations in appetite, activity, or memory for cache sites. Corticosterone or vehicle was administered to subjects 5 min prior to either caching or recovery in a naturalistic laboratory paradigm during which we recorded the number of caching events, sites visited, and seeds eaten (caching) or caches recovered, total sites visited, cache-related visits, and non-cache-related visits (recovery). Data were analyzed using nested ANOVA for treatment within sequential trial. There was no effect on any caching behaviors following treatment. However, birds treated with corticosterone during retrieval recovered more seeds and tended to visit more cache-related sites than did controls. Since groups did not differ in the number of seeds eaten or the total number of sites visited, it seems unlikely that corticosterone affected appetite or activity. Rapid surges in corticosterone may increase the efficacy of an underlying memory process for cache sites which is reflected in higher cache recovery in corticosterone-treated birds than in controls. Thus, rapid alterations in plasma corticosterone following environmental change may alter memory-reliant behaviors which promote survival in the food-caching mountain chickadee.

Animals↗

PubMed2000

The hippocampus and memory: a comparative and ethological perspective.

During the past year, considerable progress has been made in our understanding of the wide-ranging functions of the hippocampus. Highlights include the development of new tasks with which to assess spatial/topographic memory in humans and monkeys, novel tests of relational memory in rats, and episodic-like memory tasks in birds. In addition, novel theories of hippocampal function have been developed that are notable for their applicability to both humans and animal models.

Animals↗

PubMed1999

Androgen metabolism in the juvenile oscine forebrain: a cross-species analysis at neural sites implicated in memory function.

Juvenile songbirds are useful models for studying the neural bases of memory. Memory-reliant behaviors demonstrated at this stage include song learning (most songbirds) and food caching (food-storing songbirds). Sex steroids are implicated in the modulation of memory processes in several vertebrates. The songbird forebrain expresses aromatase, 5alpha-reductase and 5beta-reductase, enzymes which convert testosterone to estradiol, 5alpha-, and 5beta-dihydrotestosterone, respectively. To explore the role of local androgen metabolism on memory processes, we documented the activities of these enzymes in the anterior neostriatum (NAN), caudomedial neostriatum (NCM), and hippocampus (HP) of four species of juvenile songbird, two of which are food storers. Areas were dissected, homogenized, and provided with radiolabeled substrate; and formed estrogens, and 5alpha- and 5beta-reduced androgens were measured. In the NAN, 5beta-reductase was the predominant enzyme, suggesting that local inactivation of testosterone may preserve the sensitive period of song acquisition. In the NCM, estrogens were formed in abundance despite high 5beta-reductase, suggesting that locally high estrogen synthesis may play a role in processes of song perception. In the HP, both estrogens and 5alpha reduced androgens were formed, suggesting that HP function may be modulated by both estrogens and androgens. Finally, a derived measure of steroid-differential reveals that food-storing songbirds differ from nonstorers in the steroidal milleiu within the HP, but not in the NAN or NCM. Thus, distinct loci within the juvenile songbird forebrain are exposed to different patterns of androgen metabolites. This local conversion may play a role in the neuroendocrine modulation of memory in these birds.

Age Factors↗

PubMed1999

Analysing hippocampal function in transgenic mice: an ethological perspective.

Advances in molecular genetics and technology have led to the dawn of a new era for neuroscience: manipulation of single genes now makes it possible to dissect the complexities of neurobiological phenotypes and to understand many of the intricacies of brain and behaviour, even in mammals. The phenotypical analysis of these mutant animals is complicated because the potential outcome of gene manipulation is difficult to predict. While behavioural analysis should form an integral part of any multidisciplinary research programme investigating the phenotypical effects of single genes on hippocampal function, it is crucial that the behavioural tests are designed and conducted appropriately. Approaches that take species-specific behavioural characteristics into account and use ethological methods could be the most useful for interpreting these behavioural findings and understanding the biological mechanisms of brain function.

Animals↗

PubMed1999

Song behavior, NGF level and NPY distribution in the brain of adult male zebra finches.

The aim of the present study was to investigate the role of nerve growth factor (NGF) and neuropeptide Y (NPY) in the higher vocal center (HVC) on singing behavior of adult male zebra finches. The results of our studies show: (a) that NGF is present in the brain of these birds and it is higher in the HVC than in the other neostriatal tissues; (b) that exogenous administration of NGF or NGF-antibody had no discernible effect on singing behavior; and (c) that NGF enhances the NPY immunoreactivity in neurons and fibers localized in HVC and other areas of the neostriatum and hippocampus whereas anti-NGF decreased NPY stained cells in the hippocampus. These studies indicate that NGF is produced in the brain of zebra finch and that it plays a role in the regulation of NPY.

Animals↗

PubMed1999

Sexual dimorphism and species differences in HVC volumes of cowbirds.

Cowbirds exhibit extensive variation in their social, territorial, and reproductive behaviors. Nissl-stained brain sections of specimens from a previous study (J. C. Reboreda, N. S. Clayton, & A. Kacelnik, 1996) were used to study the gross anatomy of a song control nucleus in 3 South American cowbirds (bay-winged, Molothrus badius; shiny, M. bonariensis; and screaming, M. rufoaxillaris). Cowbird high vocal center (HVC) volumes were consistently higher in males than in females in all 3 species. The largest HVC size of females found in bay-winged cowbirds is consistent with observations that females of this species, but not of the other 2 species, occasionally sing. The extent of the sexual dimorphism of relative HVC size was highest for the sexually dichromatic and promiscuous shiny cowbirds and smaller for the monochromatic and monogamous bay-winged and screaming cowbirds, suggesting that selection pressures associated with morphological traits and social systems are reflected in brain architecture.

Animals↗

PubMed1999

Scrub jays (Aphelocoma coerulescens) remember the relative time of caching as well as the location and content of their caches.

Two experiments examined whether food-storing scrub jays (Aphelocoma coerulescens) could remember when they cached particular food items as well as what they cached and where. In Experiment 1, scrub jays cached and recovered perishable "wax worms" (wax moth larvae) and nonperishable peanuts in 2 visuospatially distinct and trial-unique trays. The birds searched preferentially for fresh wax worms if they had cached them 4 hr earlier but rapidly learned to search for peanuts and avoid decayed wax worms that had been cached 124 hr previously. This pattern also was observed when the food items were removed before recovery on test trials. These results were replicated in Experiment 2 using a procedure in which both types of food were cached in different sides of the same caching tray: On the basis of a single, trial-unique experience, scrub jays could remember the relative time of caching as well as what type of food was cached in each cache site.

Animals↗

PubMed1999

Memory for the content of caches by scrub jays (Aphelocoma coerulescens).

To test whether scrub jays (Aphelocoma coerulescens) remember the contents of food caches, in Experiment 1 birds cached peanuts and kibbles in two distinct caching trays and recovered them 4 or 172 hr later. The relative incentive value of the foods was manipulated by prefeeding one of the foods immediately before cache recovery. Birds preferentially searched for non-prefed food caches even when the caches had been pilfered prior to the recovery test. In Experiment 2, birds cached both foods in different sites within each tray, recovering peanuts from one tray and kibbles from the other tray 3 hr later. After prefeeding with one food, birds preferentially searched tray sites in which they had cached but not retrieved the non-prefed food. Thus jays remember the specific foods they cache and recover by a mnemonic process that cannot be explained in terms of simple associations between the foods and their cache locations.

Animals↗

PubMed1998

Episodic-like memory during cache recovery by scrub jays.

The recollection of past experiences allows us to recall what a particular event was, and where and when it occurred, a form of memory that is thought to be unique to humans. It is known, however, that food-storing birds remember the spatial location and contents of their caches. Furthermore, food-storing animals adapt their caching and recovery strategies to the perishability of food stores, which suggests that they are sensitive to temporal factors. Here we show that scrub jays (Aphelocoma coerulescens) remember 'when' food items are stored by allowing them to recover perishable 'wax worms' (wax-moth larvae) and non-perishable peanuts which they had previously cached in visuospatially distinct sites. Jays searched preferentially for fresh wax worms, their favoured food, when allowed to recover them shortly after caching. However, they rapidly learned to avoid searching for worms after a longer interval during which the worms had decayed. The recovery preference of jays demonstrates memory of where and when particular food items were cached, thereby fulfilling the behavioural criteria for episodic-like memory in non-human animals.

Animals↗