Neuronal activation in the geomagnetic responsive region Cluster N covaries with nocturnal migratory restlessness in white-throated sparrows (Zonotrichia albicollis).

Cluster N is a region of the visual forebrain of nocturnally migrating songbirds that supports the geomagnetic compass of nocturnal migrants. Cluster N expresses immediate-early genes (ZENK), indicating neuronal activation. This neuronal activity has only been recorded at night during the migratory season. Night-to-night variation in Cluster N activity in relation to migratory behaviour has not been previously examined. We tested whether Cluster N is activated only when birds are motivated to migrate and presumably engage their magnetic compass. We measured immediate-early gene activation in Cluster N of white-throated sparrows (Zonotrichia albicollis) in three conditions: daytime, nighttime migratory restless and nighttime resting. Birds in the nighttime migratory restlessness group had significantly greater numbers of ZENK-labelled cells in Cluster N compared to both the daytime and the nighttime resting groups. Additionally, the degree of migratory restlessness was positively correlated with the number of ZENK-labelled cells in the nighttime migratory restless group. Our study adds to the number of species observed to have neural activation in Cluster N and demonstrates for the first time that immediate early gene activation in Cluster N is correlated with the amount of active migratory behaviour displayed across sampled individuals. We conclude that Cluster N is facultatively regulated by the motivation to migrate, together with nocturnal activity, rather than obligatorily active during the migration season.

Interaction of memory systems is controlled by context in both food-storing and non-storing birds.

Animals and humans have multiple memory systems. While both black-capped chickadees (Poecile atricapillus) and dark-eyed juncos (Junco hyemalis) are under selective pressure to remember reliable long-term spatial locations (habit memory), chickadees must additionally quickly form and rapidly update spatial memory for unique cache sites (one-trial memory). We conducted a series of three experiments in which we assessed the degree to which habit and one-trial memory were expressed in both species as a function of training context. In Experiment 1, birds failed to demonstrate habits on probe trials after being trained in the context of a biased Match-to-Sample task in which the same high-frequency target was always correct. In Experiment 2, habit strongly controlled performance when habits were learned as Discriminations, defining a specific training context. In Experiment 3, context no longer defined when to express habits and habit and one-trial memory competed for control of behavior. Across all experiments, birds preferentially used the memory system at test that was consistent with the context in which it was acquired. Although the memory adaptations that allow chickadees to successfully recover cached food might predispose them to favor one-trial memory, we found no species differences in the weighting of habit and one-trial memory. In the experiments here, context was a powerful factor controlling the interaction of memory systems.

Canada jays (Perisoreus canadensis) balance protein and energy targets simultaneously in both consumed and cached food.

Food scarce periods pose serious physiological challenges for birds, especially in energetically demanding conditions. For species in the northern hemisphere, a decrease in available resources during winter adds further physiological stress to the energetic demands of life at low temperatures. Some species cache food to provide a reliable energy and nutrient resource during scarcity. Canada Jays are a year-round food-caching resident of the North American boreal forest. Canada Jays also rear their young prior to spring green up, making food caching not only essential for adult winter survival, but also potentially important for meeting the requirements of growing offspring in late winter and early spring. We examined the diet choices of Canada Jays immediately prior to winter, and the macronutrient composition of the foods Canada Jay consumed and cached at this time. We found that Canada Jays cache the same relative amounts of macronutrients as they consume but did not vary macronutrients seasonally. The similarities in the macronutrient proportions cached and consumed suggest a consistent nutrient intake pattern, and that Canada Jays are foraging to simultaneously meet similar minimum energy and minimum protein targets for both the present and future. These simultaneous targets constrain the caching decisions of jays when presented with dietary choices.

No evidence for future planning in Canada jays (Perisoreus canadensis).

In the past 20 years, research in animal cognition has challenged the belief that complex cognitive processes are uniquely human. At the forefront of these challenges has been research on mental time travel and future planning in jays. We tested whether Canada jays (Perisoreus canadensis) demonstrated future planning, using a procedure that has produced evidence of future planning in California scrub-jays. Future planning in this procedure is caching in locations where the bird will predictably experience a lack of food in the future. Canada jays showed no evidence of future planning in this sense and instead cached in the location where food was usually available, opposite to the behaviour described for California scrub-jays. We provide potential explanations for these differing results adding to the recent debates about the role of complex cognition in corvid caching strategies.

Black-capped chickadees (Poecile atricapillus) use temperature as a cue for reproductive timing.

Reliable environmental cues, such as photoperiod, act as initial predictive cues that allow birds to time reproduction to match peak food abundance for their offspring. More variable local cues, like temperature, may, however, provide more precise information about the timing of food abundance. Non-migratory birds, in particular, should be sensitive to temperature cues and use them to modulate their reproductive timing. We conducted two experiments to examine the effect of temperature on reproductive condition (gonad size and circulating androgen levels) in non-migratory black-capped chickadees (Poecile atricapillus). First, we exposed groups of birds in outdoor aviaries to three different over-winter temperature treatments and assessed gonad size in the spring. Second, we manipulated temperature in environmental chambers under photostimulatory and non-photostimulatory photoperiodic conditions and assessed gonad size and circulating testosterone levels. Temperature had no independent effect on gonad size or testosterone levels, but when photostimulated birds exposed to warmer conditions became reproductively ready earlier than birds experiencing cooler conditions. We conclude that temperature acts as a supplementary cue that modulates the photoperiod-driven timing of reproduction.

Imidacloprid impairs performance on a model flower handling task in bumblebees (Bombus impatiens).

Bumblebees exposed to neonicotinoid pesticides collect less pollen on foraging trips. Exposed bumblebees are also slower to learn to handle flowers, which may account for reduced pollen collection. It is unclear, however, why neonicotinoid exposure slows learning to handle flowers. We investigated the effect of imidacloprid, a neonicotinoid pesticide, on bumblebee motor learning using a lab model of flower handling. Bumblebees learned to invert inside a narrow tube and lift a petal-shaped barrier to reach a reward chamber. Imidacloprid-exposed bumblebees showed a dose-dependent delay to solve the task, which resulted from reduced switching between behavioural strategies and a subsequent delay in use of the successful strategy. This effect was consistent in colonies exposed at 10 but not 2.6 ppb, suggesting a variable effect on individuals at lower doses. These results help to explain why exposed bumblebees are slow to learn to handle flowers and collect less pollen on foraging trips.

Imidacloprid slows the development of preference for rewarding food sources in bumblebees (Bombus impatiens).

Bee pollination is economically and ecologically vital and recent declines in bee populations are therefore a concern. One possible cause of bee declines is pesticide use. Bumblebees exposed to imidacloprid, a neonicotinoid pesticide, have been shown to be less efficient foragers and collect less pollen on foraging trips than unexposed bees. We investigated whether bumblebees (Bombus impatiens) chronically exposed to imidacloprid at field-realistic levels of 2.6 and 10 ppb showed learning deficits that could affect foraging. Bumblebees were tested for their ability to associate flower colour with reward value in a simulated foraging environment. Bumblebees completed 10 foraging trips in which they collected sucrose solution from artificial flowers that varied in sucrose concentration. The reward quality of each artificial flower was predicted by corolla colour. Unexposed bumblebees acquired a preference for feeding on the most rewarding flower colour on the second foraging trip, while bumblebees exposed at 2.6 and 10 ppb did not until their third and fifth trip, respectively. The delay in preference acquisition in exposed bumblebees may be due to reduced flower sampling and shorter foraging trips. These results show that bumblebees exposed to imidacloprid are slow to learn the reward value of flowers and this may explain previously observed foraging inefficiencies associated with pesticide exposure.

Are There Place Cells in the Avian Hippocampus?

Birds possess a hippocampus that serves many of the same spatial and mnemonic functions as the mammalian hippocampus but achieves these outcomes with a dramatically different neuroanatomical organization. The properties of spatially responsive neurons in birds and mammals are also different. Much of the contemporary interest in the role of the mammalian hippocampus in spatial representation dates to the discovery of place cells in the rat hippocampus. Since that time, cells that respond to head direction and cells that encode a grid-like representation of space have been described in the rat brain. Research with homing pigeons has discovered hippocampal cells, including location cells, path cells, and pattern cells, that share some but not all properties of spatially responsive neurons in the rodent brain. We have recently used patterns of immediate-early gene expression, visualized by the catFISH method, to investigate how neurons in the hippocampus of brood-parasitic brown-headed cowbirds respond to spatial context. We have found cells that discriminate between different spatial environments and are re-activated when the same spatial environment is re-experienced. Given the differences in habitat and behaviour between birds and rodents, it is not surprising that spatially responsive cells in their hippocampus and other brain regions differ. The enormous diversity of avian habitats and behaviour offers the potential for understanding the general principles of neuronal representation of space.

Seasonal change in the avian hippocampus.

The hippocampus plays an important role in cognitive processes, including memory and spatial orientation, in birds. The hippocampus undergoes seasonal change in food-storing birds and brood parasites, there are changes in the hippocampus during breeding, and further changes occur in some species in association with migration. In food-storing birds, seasonal change in the hippocampus occurs in fall and winter when the cognitively demanding behaviour of caching and retrieving food occurs. The timing of annual change in the hippocampus of food-storing birds is quite variable, however, and appears not to be under photoperiod control. A variety of factors, including cognitive performance, exercise, and stress may all influence seasonal change in the avian hippocampus. The causal processes underlying seasonal change in the avian hippocampus have not been extensively examined and the more fully described hormonal influences on the mammalian hippocampus may provide hypotheses for investigating the control of hippocampal seasonality in birds.

Site-specific regulation of adult neurogenesis by dietary fatty acid content, vitamin E and flight exercise in European starlings.

Exercise is known to have a strong effect on neuroproliferation in mammals ranging from rodents to humans. Recent studies have also shown that fatty acids and other dietary supplements can cause an upregulation of neurogenesis. It is not known, however, how exercise and diet interact in their effects on adult neurogenesis. We examined neuronal recruitment in multiple telencephalic sites in adult male European starlings (Sturnus vulgaris) exposed to a factorial combination of flight exercise, dietary fatty acids and antioxidants. Experimental birds were flown in a wind tunnel following a training regime that mimicked the bird's natural flight behaviour. In addition to flight exercise, we manipulated the composition of dietary fatty acids and the level of enrichment with vitamin E, an antioxidant reported to enhance neuronal recruitment. We found that all three factors - flight exercise, fatty acid composition and vitamin E enrichment - regulate neuronal recruitment in a site-specific manner. We also found a robust interaction between flight training and vitamin E enrichment at multiple sites of neuronal recruitment. Specifically, flight training was found to enhance neuronal recruitment across the telencephalon, but only in birds fed a diet with a low level of vitamin E. Conversely, dietary enrichment with vitamin E upregulated neuronal recruitment, but only in birds not flown in the wind tunnel. These findings indicate conserved modulation of adult neurogenesis by exercise and diet across vertebrate taxa and indicate possible therapeutic interventions in disorders characterized by reduced adult neurogenesis.

Serial reversal learning in bumblebees (Bombus impatiens).

Bumblebees are capable of rapidly learning discriminations, but flexibility in bumblebee learning is less well understood. We tested bumblebees (Bombus impatiens) on a serial reversal learning task. A serial reversal task requires learning of an initial discrimination between two differentially rewarded stimuli, followed by multiple reversals of the reward contingency between stimuli. A reduction in errors with repeated reversals in a serial reversal task is an indicator of behavioural flexibility. Bees were housed in a large indoor environment and tested during foraging flights. Testing free-flying bees allowed for large numbers of trials and reversals. All bees were trained to perform a simultaneous discrimination between two colours for a nectar reward, followed by nine reversals of this discrimination. Results showed that bumblebees reduced errors and improved their performance across successive reversals. A reduction in perseverative errors was the major cause of the improvement in performance. Bees showed a slight increase in error rate in their final trials, perhaps as a consequence of increasing proactive interference, but proactive interference may also have contributed to the overall improvement in performance across reversals. Bumblebees are thus capable of behavioural flexibility comparable to that of other animals and may use proactive interference as a mechanism of behavioural flexibility in varying environments.

Female cowbirds have more accurate spatial memory than males.

Brown-headed cowbirds (Molothrus ater) are obligate brood parasites. Only females search for host nests and they find host nests one or more days before placing eggs in them. Past work has shown that females have a larger hippocampus than males, but sex differences in spatial cognition have not been extensively investigated. We tested cowbirds for sex and seasonal differences in spatial memory on a foraging task with an ecologically relevant retention interval. Birds were trained to find one rewarded location among 25 after 24 h. Females made significantly fewer errors than males and took more direct paths to the rewarded location than males. Females and males showed similar search times, indicating there was no sex difference in motivation. This sex difference in spatial cognition is the reverse of that observed in some polygynous mammals and is consistent with the hypothesis that spatial cognition is adaptively specialized in this brood-parasitic species.

Social learning: nectar robbing spreads socially in bumble bees.

Social transmission of learned behaviour is well documented in vertebrates but much less so among invertebrates. New research shows that nectar robbing can spread socially among bumble bees, even in the absence of nectar-robbing models.

Interval timing by an invertebrate, the bumble bee Bombus impatiens.

Sensitivity to temporal information and the ability to adjust behavior to the temporal structure of the environment should be phylogenetically widespread. Some timing abilities, such as sensitivity to circadian cycles, appear in a wide range of invertebrate and vertebrate taxa [1,2]. Interval timing--sensitivity to the duration of time intervals--has, however, only been shown to occur in vertebrates [3,4]. Insect pollinators make a variety of decisions that would appear to require the ability to estimate elapsed durations. We exposed bumble bees to conditions in which proboscis extension was reinforced after a fixed duration had elapsed or after either of two fixed durations had elapsed. Two groups of bees were trained with a short duration (either 6 s or 12 s) and a long duration (36 s) in separate experimental phases (independent timing groups), whereas two other groups were trained with a short duration (either 6 s or 12 s) and long duration (36 s) always intermixed unpredictably (multiple timing groups). On long intervals, independent timing groups waited longer than mixed timing groups to generate the first response and responded maximally near the end of the interval. Multiple timing groups waited the same amount of time on average before generating the first response on both long and short intervals. On individual trials, multiple timing groups appeared to time either the long duration only or both the short and long durations: most trials were characterized by a single burst of responding that began between the short and long duration values or by two bursts of responding with the first burst bracketing the short value and the second burst beginning in anticipation of the long value. These results show that bumble bees learn to time interval durations and can flexibly time multiple durations simultaneously. The results indicate no phylogenetic divide between vertebrates and invertebrates in interval timing ability.

Memory for what, where, and when in the black-capped chickadee (Poecile atricapillus).

Episodic memory is the ability to remember personally experienced past events (Tulving in Organization of memory. Academic Press, San Diego, pp. 381-403, 1972). In non-human animals, the behavioural criterion for episodic-like memory is remembering "what" occurred in conjunction with "when" and "where" (Clayton and Dickinson in Nature 395:272-274, 1998). We conducted tests for "what, where, and when" memory in a food-storing bird, the black-capped chickadee (Poecile atricapillus). In Experiment 1, chickadees found sunflower seeds and mealworms in concealed sites in their home cage. Birds later re-visited these sites after either a short (3 h) or long (123 h) retention interval. Chickadees normally prefer mealworms, but at the long retention interval mealworms were degraded in taste and appearance. Chickadees showed some memory for what kind of food they had encountered and where, but no memory for when food had previously been found. Experiment 2 followed a similar procedure, except that chickadees searched for hidden sunflower seeds and mealworms in trees in an indoor aviary. These more natural conditions increased both the spatial scale of the task and the effort required to find food. In this experiment, birds showed evidence for all three components of what-where-when memory. Unlike some previous studies of episodic-like memory, birds' behaviour cannot be accounted for by differential memory strength for more recent events. The results show that memory for what, where, and when occurs in food-storing birds outside the corvid family, does not require food caching or retrieval, and that remembering "when" can depend on the nature of the task.

Cognition and the brain of brood parasitic cowbirds.

Cowbirds are brood parasites. Females lay their eggs in the nests of other species, which then incubate the cowbird eggs and raise the young cowbirds. Finding and returning to heterospecific nests presents cowbirds with several cognitive challenges. In some species, such as brown-headed cowbirds (Molothrus ater), females but not males search for and remember the locations of potential host nests. We describe recent research on sex differences in cognition and the hippocampus associated with this sex difference in search for host nests. Female brown-headed cowbirds perform better than males on some, but not all, tests of spatial memory and females show a pattern of adult hippocampal neurogenesis not found in males or in closely related non-parasitic birds. Because of the apparent specialization of the hippocampus, brown-headed cowbirds may be a good model in which to examine spatial information processing in the avian hippocampus and we also describe recent research on the spatial response properties of brown-headed cowbird hippocampal neurons.

Overwinter temperature has no effect on problem solving abilities or responses to novelty in Black-capped Chickadees (Poecile atricapillus).

Birds overwintering at northern latitudes face challenging environments in which refined cognitive and behavioural responses to environmental stimuli could be a benefit. Populations of the same species from different latitudes have been shown to differ in their cognitive and behavioural responses, and these differences have been attributed to local adaptation. However, individuals overwintering at intermediate latitudes experience great breadth and variation in environmental conditions, and thus it is reasonable that these individuals would alter their responses based on current conditions. To determine within-species responses to environmental conditions we sampled birds from a single population at an intermediate latitude and assessed their problem solving abilities and their responses to novelty. We held birds overwinter in one of three experimental temperature regimes and assessed problem solving abilities and responses to novel stimuli in the spring. We found that overwinter temperature had no effect on problem solving ability. We also show that overwinter temperature had no effect on an individual's response to novelty. These findings strengthen the argument that differences in these behaviours seen at the population level are in fact driven by local adaptation, and that current environmental condition may have limited effects on these behaviours.

Decreased Neurogenesis Increases Spatial Reversal Errors in Chickadees (Poecile atricapillus).

Adult hippocampal neurogenesis has been proposed to both aid memory formation and disrupt memory. We examined the role of adult hippocampal neurogenesis in spatial working and reference memory in black-capped chickadees (Poecile atricapillus), a passerine bird that relies on spatial memory for cache retrieval and foraging. We tested spatial working and spatial reference memory in birds that had received methylazoxymethanol acetate (MAM), a neurotoxin that decreases hippocampal neurogenesis. MAM treatment significantly reduced neurogenesis in the hippocampus quantified by doublecortin (DCX) labeling of newly divided and migrating neurons. MAM treatment had little effect on the working or reference memory but caused an increase in errors on the reference memory task following reversal. Working memory for recently visited spatial locations and reference memory for familiar spatial locations were thus unaffected by a reduction in neurogenesis. An increase in errors following reference memory reversal may indicate that adult hippocampal neurogenesis aids in pattern separation, the differentiation of similar memories at the time of encoding.

Floral reward production is timed by an insect pollinator.

Interval timing--sensitivity to elapsing durations--has recently been found to occur in an invertebrate pollinator, the bumble-bee (Bombus impatiens). Here, bumble-bees were required to time the interval between the start of foraging in a patch of low-quality artificial flowers providing 25% sucrose and the availability of a high-quality flower (HQF) that provided 50% sucrose after a fixed delay. The delay changed after every 20 foraging bouts in the order 30-150-30 s. Bees visited the HQF sooner when the delay was 30 s than when it was 150 s, and visits to the HQF peaked near the end of both delays. When the delay changed to 150 s, bees appeared to time both the previous 30 s delay and the new delay. To examine whether bees also learned what kind of reward was provided at the HQF, its usual reward was replaced with 25% sucrose in a final foraging bout. Bumble-bees rejected the HQF on the reward-replacement test. These results show that bumble-bees remembered both when reward was produced by the HQF and what type of reward was produced. These findings indicate that bumble-bees can learn both the timing and content of reward production.

Annual cycle of the black-capped chickadee: seasonality of food-storing and the hippocampus.

Previous research presents a mixed picture of seasonal variation in the hippocampus of food-storing black-capped chickadees. One field study has shown an October peak in hippocampus volume, although laboratory studies conducted to determine whether photoperiod regulates this seasonal growth have failed to find changes in the size of the hippocampus. To resolve the discrepancy between field and lab reports we examined caching activity, hippocampal volume, and neurogenesis in adult male black-capped chickadees at four times over the annual cycle: October, January, April and July. We found that more birds stored food in October than at other times of year, but did not observe a significant change in the size of the hippocampus over the annual cycle. Telencephalon volume, however, was larger in October than in July. Hippocampal neuronal recruitment showed a significant peak in January, but there was no seasonal change in neuronal recruitment in the adjacent hyperpallium apicale. These results indicate that there might be seasonal variation in the recruitment of new neurons into the hippocampus of chickadees without overall seasonal change in hippocampal size.