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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

Hippocampal Astrocytes in Migrating and Wintering Semipalmated Sandpiper Calidris pusilla.

Seasonal migratory birds return to the same breeding and wintering grounds year after year, and migratory long-distance shorebirds are good examples of this. These tasks require learning and long-term spatial memory abilities that are integrated into a navigational system for repeatedly locating breeding, wintering, and stopover sites. Previous investigations focused on the neurobiological basis of hippocampal plasticity and numerical estimates of hippocampal neurogenesis in birds but only a few studies investigated potential contributions of glial cells to hippocampal-dependent tasks related to migration. Here we hypothesized that the astrocytes of migrating and wintering birds may exhibit significant morphological and numerical differences connected to the long-distance flight. We used as a model the semipalmated sandpiper Calidris pusilla, that migrates from northern Canada and Alaska to South America. Before the transatlantic non-stop long-distance component of their flight, the birds make a stopover at the Bay of Fundy in Canada. To test our hypothesis, we estimated total numbers and compared the three-dimensional (3-D) morphological features of adult C. pusilla astrocytes captured in the Bay of Fundy (n = 249 cells) with those from birds captured in the coastal region of Bragança, Brazil, during the wintering period (n = 250 cells). Optical fractionator was used to estimate the number of astrocytes and for 3-D reconstructions we used hierarchical cluster analysis. Both morphological phenotypes showed reduced morphological complexity after the long-distance non-stop flight, but the reduction in complexity was much greater in Type I than in Type II astrocytes. Coherently, we also found a significant reduction in the total number of astrocytes after the transatlantic flight. Taken together these findings suggest that the long-distance non-stop flight altered significantly the astrocytes population and that morphologically distinct astrocytes may play different physiological roles during migration.

Context-Dependent Egr1 Expression in the Avian Hippocampus.

In mammals, episodic memory and spatial cognition involve context-specific recruitment of unique ensembles in the hippocampal formation (HF). Despite their capacity for sophisticated spatial (e.g., for migration) and episodic-like (e.g., for food-caching) memory, the mechanisms underlying contextual representation in birds is not well understood. Here we demonstrate environment-specific Egr1 expression as male brown-headed cowbirds (Molothrus ater) navigate environments for food reward, showing that the avian HF, like its mammalian counterpart, recruits distinct neuronal ensembles to represent different contexts.

Sex and seasonal differences in hippocampal volume and neurogenesis in brood-parasitic brown-headed cowbirds (Molothrus ater).

Brown-headed cowbirds (Molothrus ater) are one of few species in which females show more complex space use than males. Female cowbirds search for, revisit, and parasitize host nests and, in a previous study, outperformed males on an open field spatial search task. Previous research reported a female-biased sex difference in the volume of the hippocampus, a region of the brain involved in spatial memory. Neurons produced by adult neurogenesis may be involved in the formation of new memories and replace older neurons that could cause interference in memory. We tested for sex and seasonal differences in hippocampal volume and neurogenesis of brood-parasitic brown-headed cowbirds and the closely related non-brood-parasitic red-winged blackbird (Agelaius phoeniceus) to determine whether there were differences in the hippocampus that reflected space use in the wild. Females had a larger hippocampus than males in both species, but hippocampal neurogenesis, measured by doublecortin immunoreactivity (DCX+), was greater in female than in male cowbirds in the absence of any sex difference in blackbirds, supporting the hypothesis of hippocampal specialization in female cowbirds. Cowbirds of both sexes had a larger hippocampus with greater hippocampal DCX+ than blackbirds. Hippocampus volume remained stable between breeding conditions, but DCX+ was greater post-breeding, indicating that old memories may be lost through hippocampal reorganization following breeding. Our results support, in part, the hypothesis that the hippocampus of cowbirds is specialized for brood parasitism. © 2016 Wiley Periodicals, Inc. Develop Neurobiol 76: 1275-1290, 2016.

Sex and seasonal differences in neurogenesis and volume of the song-control system are associated with song in brood-parasitic and non-brood-parasitic icterid songbirds.

The song-control system in the brain of songbirds is important for the production and acquisition of song and exhibits both remarkable seasonal plasticity and some of the largest neural sex differences observed in vertebrates. We measured sex and seasonal differences in two nuclei of the song-control system of brood-parasitic brown-headed cowbirds (Molothrus ater) and closely-related non-parasitic red-winged blackbirds (Agelaius phoeniceus). These species differ in both the development and function of song. Brown-headed cowbirds have a larger sex difference in song than red-winged blackbirds. Female cowbirds never sing, whereas female blackbirds do though much less than males. In cowbirds, song primarily functions in mate choice and males modify their song as they approach sexual maturity and interact with females. In red-winged blackbirds, song is used primarily in territorial defence and is crystalized earlier in life. We found that the HVC was more likely to be discernable in breeding female blackbirds than in breeding female cowbirds. Compared to males, females had a smaller HVC and a smaller robust nucleus of the arcopallium (RA). However, females had higher doublecortin immunoreactivity (DCX+) in HVC, a measure of neurogenesis. Consistent with sex differences in song, the sex difference in RA volume was greater in cowbirds than in blackbirds. Males of both species had a smaller HVC with higher DCX+ in post-breeding condition than in breeding condition when song is more plastic. Sex and seasonal differences in the song-control system were closely related to variation in song in these two icterid songbirds. © 2016 Wiley Periodicals, Inc. Develop Neurobiol 76: 1226-1240, 2016.

Sex Differences in Spatial Memory in Brown-Headed Cowbirds: Males Outperform Females on a Touchscreen Task.

Spatial cognition in females and males can differ in species in which there are sex-specific patterns in the use of space. Brown-headed cowbirds are brood parasites that show a reversal of sex-typical space use often seen in mammals. Female cowbirds, search for, revisit and parasitize hosts nests, have a larger hippocampus than males and have better memory than males for a rewarded location in an open spatial environment. In the current study, we tested female and male cowbirds in breeding and non-breeding conditions on a touchscreen delayed-match-to-sample task using both spatial and colour stimuli. Our goal was to determine whether sex differences in spatial memory in cowbirds generalizes to all spatial tasks or is task-dependant. Both sexes performed better on the spatial than on the colour touchscreen task. On the spatial task, breeding males outperformed breeding females. On the colour task, females and males did not differ, but females performed better in breeding condition than in non-breeding condition. Although female cowbirds were observed to outperform males on a previous larger-scale spatial task, males performed better than females on a task testing spatial memory in the cowbirds' immediate visual field. Spatial abilities in cowbirds can favour males or females depending on the type of spatial task, as has been observed in mammals, including humans.

Contrasting styles in cognition and behaviour in bumblebees and honeybees.

Bumblebees and honeybees have been the subjects of a great deal of recent research in animal cognition. Many of the major topics in cognition, including memory, attention, concept learning, numerosity, spatial cognition, timing, social learning, and metacognition have been examined in bumblebees, honeybees, or both. Although bumblebees and honeybees are very closely related, they also differ in important ways, including social organization, development, and foraging behaviour. We examine whether differences between bumblebees and honeybees in cognitive processes are related to differences in their natural history and behaviour. There are differences in some cognitive traits, such as serial reversal learning and matching-to-sample, that appear related to differences between bumblebees and honeybees in foraging and social behaviour. Other cognitive processes, such as numerosity, appear to be very similar. Despite the wealth of information that is available on some aspects of bumblebee and honeybee cognition and behaviour, there are relatively few instances, however, in which adequate data exist to make direct comparisons. We highlight a number of phenomena, including concept learning, spatial cognition, timing, and metacognition, for which targeted comparative research may reveal unexpected adaptive variation in cognitive processes in these complex animals. This article is part of a Special Issue entitled: In Honor of Jerry Hogan.

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.

Inhibition of cell proliferation in black-capped chickadees suggests a role for neurogenesis in spatial learning.

Following development, the avian brain continues to produce neurons throughout adulthood, which functionally integrate throughout the telencephalon, including the hippocampus. In food-storing birds like the black-capped chickadee (Poecile atricapillus), new neurons incorporated into the hippocampus are hypothesized to play a role in spatial learning. Previous results on the relation between hippocampal neurogenesis and spatial learning, however, are correlational. In this study, we experimentally suppressed hippocampal neuronal recruitment and tested for subsequent effects on spatial learning in adult chickadees. After chickadees exhibited significant learning, we treated birds with daily injections of either saline or methylazoxymethanol (MAM), a toxin that suppresses cell proliferation in the brain and monitored subsequent spatial learning. MAM treatment significantly reduced cell proliferation around the lateral ventricles and neuronal recruitment in the hippocampus, measured using the cell birth marker bromodeoxyuridine. MAM-treated birds performed significantly worse than controls on the spatial learning task 12 days following the initiation of MAM treatment, a time when new neurons would begin functionally integrating into the hippocampus. This difference in learning, however, was limited to a single trial. MAM treatment did not affect any measure of body condition, suggesting learning impairments were not a product of non-specific adverse effects of MAM. This is the first evidence of a potential causal link between hippocampal neurogenesis and spatial learning in birds.

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.