Food-storing birds: adaptive specialization in brain and behaviour?

Among the passerine birds, species that store food have an enlarged hippocampal region (dorso-medial cortex), relative to brain and body size, when compared with the non-storers. The volume of one of the major afferent-efferent pathways (the septo-hippocampal pathway) is also greater in food storing species. This specialization of brain structure is discussed in relation to behavioural studies in which the spatial memory of storing and non-storing species has been compared.     

Septum volume and food-storing behavior are related in parids

The hippocampal formation (HF) of food-storing birds is larger than non-storing species, and the size of the HF in food-storing Black-Capped Chickadees (Poecile atricapillus) varies seasonally. We examined whether the volume of the septum, a medial forebrain structure that shares reciprocal connections with the HF, demonstrates the same species and seasonal variation as has been shown in the HF. We compared septum volume in three parid species; non-storing Blue Tits (Parus caeruleus) and Great Tits (Parus major), and food-storing Black-Capped Chickadees. We found the relative septum volume to be larger in chickadees than in the non-storing species. We also compared septum and nucleus of the diagonal band (NDB) volume of Black-Capped Chickadees at different times of the year. We found that the relative septum volume varies seasonally in food-storing birds. The volume of the NDB does not vary seasonally. Due to the observed species and seasonal variation, the septum, like the hippocampal formation of food-storing birds, may be specialized for some aspects of food-storing and spatial memory.     

Behavior and spatial learning in birds in radial maze

Studies of spatial learning and memory of birds in radial maze are reviewed. The radial maze variants (standard, giant and open-field analog) are described; procedural problems of bird testing are discussed. Radial maze task performance of birds is compared with that of laboratory rats as a well-studied standard. Specific features of spatial learning in various taxonomic avian groups (pigeon, tits, corvids, chickens and others) are considered. The results of spatial memory studies in closely-related species with different ecology (food storing behavior, degree of caching specialization) and experiments with migrant birds and homing pigeons are discussed.     

Cognitive ornithology: the evolution of avian intelligence

Comparative psychologists interested in the evolution of intelligence have focused their attention on social primates, whereas birds tend to be used as models of associative learning. However, corvids and parrots, which have forebrains relatively the same size as apes, live in complex social groups and have a long developmental period before becoming independent, have demonstrated ape-like intelligence. Although, ornithologists have documented thousands of hours observing birds in their natural habitat, they have focused their attention on avian behaviour and ecology, rather than intelligence. This review discusses recent studies of avian cognition contrasting two different approaches; the anthropocentric approach and the adaptive specialization approach. It is argued that the most productive method is to combine the two approaches. This is discussed with respects to recent investigations of two supposedly unique aspects of human cognition; episodic memory and theory of mind. In reviewing the evidence for avian intelligence, corvids and parrots appear to be cognitively superior to other birds and in many cases even apes. This suggests that complex cognition has evolved in species with very different brains through a process of convergent evolution rather than shared ancestry, although the notion that birds and mammals may share common neural connectivity patterns is discussed.     

Memory for spatial and object-specific cues in food-storing and non-storing birds

Two storer/non-storer pairs of species, marsh tit (Parus palustris)/blue tit (P. caeruleus) and jay (Garrulus glandarius)/jackdaw (Corvus monedula) were compared on a one-trial associative memory task. In phase I of a trial birds searched for a reward in one of four feeders which differed in their trial-unique spatial location and object-specific cues. Following a retention interval, the birds had to return to the same feeder to obtain a further reward. In control trials the array of feeders was unaltered, whilst in dissociation tests it was transformed to separate spatial location and object-specific cues.In control trials there was no difference in performance between species. In dissociation tests, the two storing species went first to the correct spatial location and second to the correct object-specific cues, whereas the two non-storing species went first with equal probability to the correct spatial and local object cues.Monocular occlusion was used to investigate differences between the two eye-systems. In control trials there was no effect of occlusion. In dissociation trials, all 4 species preferentially returned to the feeder with the correct object-specific cue when the left eye had been covered in phase I and to the feeder in the correct spatial position when the right eye had been covered in phase I.These results suggest that (a) food-storing birds differ from non-storers in responding preferentially to spatial information and (b) in storers and non-storers the right eye system shows a preference for object-specific cues and the left eye system for spatial cues.     

The impact of flavonoids on spatial memory in rodents: from behaviour to underlying hippocampal mechanisms

Emerging evidence suggests that a group of dietary-derived phytochemicals known as flavonoids are able to induce improvements in memory, learning and cognition. Flavonoids have been shown to modulate critical neuronal signalling pathways involved in processes of memory, and therefore are likely to affect synaptic plasticity and long-term potentiation mechanisms, widely considered to provide a basis for memory. Animal dietary supplementation studies have further shown that flavonoid-rich foods are able to reverse age-related spatial memory and spatial learning impairments. A more accurate understanding of how a particular spatial memory task works and of which aspects of memory and learning can be assessed in each case, are necessary for a correct interpretation of data relating to diet-cognition experiments. Further understanding of how specific behavioural tasks relate to the functioning of hippocampal circuitry during learning processes might be also elucidative of the specific observed memory improvements. The overall goal of this review is to give an overview of how the hippocampal circuitry operates as a memory system during behavioural tasks, which we believe will provide a new insight into the underlying mechanisms of the action of flavonoids on cognition.     

Taxonomic counts of cognition in the wild

In 1985, Kummer & Goodall pleaded for an ecology of intelligence and proposed that innovations might be a good way to measure cognition in the wild. Counts of innovation per taxonomic group are now available in hundreds of avian and primate species, as are counts of tactical deception, tool use and social learning. Robust evidence suggests that innovation rate and its neural correlates allow birds and mammals to cope better with environmental change. The positive correlations between taxonomic counts, and the increasing number of cognitive and neural measures found to be associated with ecological variables, suggest that domain general processes might be more pervasive than previously thought in the evolution of intelligence.     

Spatial ability is impaired and hippocampal mineralocorticoid receptor mRNA expression reduced in zebra finches (Taeniopygia guttata) selected for acute high corticosterone response to stress

In mammals, stress hormones have profound influences on spatial learning and memory. Here, we investigated whether glucocorticoids influence cognitive abilities in birds by testing a line of zebra finches selectively bred to respond to an acute stressor with high plasma corticosterone (CORT) levels. Cognitive performance was assessed by spatial and visual one-trial associative memory tasks. Task performance in the high CORT birds was compared with that of the random-bred birds from a control breeding line. The birds selected for high CORT in response to an acute stressor performed less well than the controls in the spatial task, but there were no significant differences between the lines in performance during the visual task. The birds from the two lines did not differ in their plasma CORT levels immediately after the performance of the memory tasks; nevertheless, there were significant differences in peak plasma CORT between the lines. The high CORT birds also had significantly lower mineralocorticoid receptor mRNA expression in the hippocampus than the control birds. There was no measurable difference between the lines in glucocorticoid receptor mRNA density in either the hippocampus or the paraventricular nucleus. Together, these findings provide evidence to suggest that stress hormones have important regulatory roles in avian spatial cognition.     

Lateralization and unilateral transfer of spatial memory in marsh tits

Summary The results reported in this paper demonstrate lateralization and transfer of spatial memory processing in an adult, food-storig bird. The technique of monocular occlusion was used to investigate lateralization and memory transfer in food-storing marsh tits (Parus palustris) for two tasks, food-storing and one-trial associative learning, which rely on one-trial learning for the spatial location of hidden food items. In the food-storing task, marsh tits had to return to the sites where they had previously stored a seed; in the one-trial associative learning task, the birds had to return to sites where they had been allowed to eat some, but not all, of a piece of peanut. For both spatial memory tasks, it was demonstrated that although the visual systems fed by both eyes are involved in short-term storage, the right eye system is associated with long-term storage, and that memories are transferred from the left to the right eye system between 3 and 24 h after memory formation.     

Septum volume and food‐storing behavior are related in parids

The hippocampal formation (HF) of food‐storing birds is larger than non‐storing species, and the size of the HF in food‐storing Black‐Capped Chickadees (Poecile atricapillus) varies seasonally. We examined whether the volume of the septum, a medial forebrain structure that shares reciprocal connections with the HF, demonstrates the same species and seasonal variation as has been shown in the HF. We compared septum volume in three parid species; non‐storing Blue Tits (Parus caeruleus) and Great Tits (Parus major), and food‐storing Black‐Capped Chickadees. We found the relative septum volume to be larger in chickadees than in the non‐storing species. We also compared septum and nucleus of the diagonal band (NDB) volume of Black‐Capped Chickadees at different times of the year. We found that the relative septum volume varies seasonally in food‐storing birds. The volume of the NDB does not vary seasonally. Due to the observed species and seasonal variation, the septum, like the hippocampal formation of food‐storing birds, may be specialized for some aspects of food‐storing and spatial memory. © 2002 Wiley Periodicals, Inc. J Neurobiol 51: 215–222, 2002     

Are cognition and personality related in budgerigars?

In recent years, researchers have been attempting to relate differences in personality (e.g., boldness, aggressiveness, exploration tendency) to variation in cognition (performances in tasks that require learning, reasoning, attention, or memory, etc.) both theoretically and empirically. However, it is unclear on what basis personality and cognition might be associated with each other. Previous theory suggests a connection between fast–slow personality types and cognitive speed–accuracy tradeoffs. In this study, we tested this hypothesis in budgerigars and found that, in their 1st associative learning, birds with fast personality (less fearful of handling stress) were fast learners in the beginning, while slow personality individuals improved faster, but both types of birds did not differ in accuracy. However, these relationships were context-dependent. No significant relationship was found in subsequent learning tasks (reversal learning and a 2nd associative learning) in the familiar context (task setup and apparatus similar to the 1st associative learning). We then conducted a problem-solving experiment with novel setup and apparatus to test 1 possible explanation that the association between personality and cognition in the 1st associative learning might be caused by noncognitive constraint, such as fearfulness when facing novel task setup and apparatus. We found that fast individuals interacted more with the problem box and solved it, whereas the slow birds were not. We suggest that personalities can influence cognitive performances and trigger a cognitive speed-improvement tradeoff under the novel context. However, there are no consistent cognitive styles that co-varied with different personalities.     

Learning outdoors: male lizards show flexible spatial learning under semi-natural conditions

Spatial cognition is predicted to be a fundamental component of fitness in many lizard species, and yet some studies suggest that it is relatively slow and inflexible. However, such claims are based on work conducted using experimental designs or in artificial contexts that may underestimate their cognitive abilities. We used a biologically realistic experimental procedure (using simulated predatory attacks) to study spatial learning and its flexibility in the lizard Eulamprus quoyii in semi-natural outdoor enclosures under similar conditions to those experienced by lizards in the wild. To evaluate the flexibility of spatial learning, we conducted a reversal spatial-learning task in which positive and negative reinforcements of learnt spatial stimuli were switched. Nineteen (32%) male lizards learnt both tasks within 10 days (spatial task mean: 8.16 ± 0.69 (s.e.) and reversal spatial task mean: 10.74 ± 0.98 (s.e.) trials). We demonstrate that E. quoyii are capable of flexible spatial learning and suggest that future studies focus on a range of lizard species which differ in phylogeny and/or ecology, using biologically relevant cognitive tasks, in an effort to bridge the cognitive divide between ecto- and endotherms.     

Seasonal hippocampal plasticity in food-storing birds

Both food-storing behaviour and the hippocampus change annually in food-storing birds. Food storing increases substantially in autumn and winter in chickadees and tits, jays and nutcrackers and nuthatches. The total size of the chickadee hippocampus increases in autumn and winter as does the rate of hippocampal neurogenesis. The hippocampus is necessary for accurate cache retrieval in food-storing birds and is much larger in food-storing birds than in non-storing passerines. It therefore seems probable that seasonal change in caching and seasonal change in the hippocampus are causally related. The peak in recruitment of new neurons into the hippocampus occurs before birds have completed food storing and cache retrieval for the year and may therefore be associated with spacing caches, encoding the spatial locations of caches, or creating a neuronal architecture involved in the recollection of cache sites. The factors controlling hippocampal plasticity in food-storing birds are not well understood. Photoperiodic manipulations that produce change in food-storing behaviour have no effect on either hippocampal size or neuronal recruitment. Available evidence suggests that changes in hippocampal size and neurogenesis may be a consequence of the behavioural and cognitive involvement of the hippocampus in storing and retrieving food.     

Estrogens and cognition: Friends or foes?: An evaluation of the opposing effects of estrogens on learning and memory

This article is part of a Special Issue “Estradiol and cognition”.Estrogens are becoming well known for their robust enhancement on cognition particularly for learning and memory that relies upon functioning of the hippocampus and related neural systems. What is also emerging is that estrogen modulation of cognition is not uniform, at times enhancing yet at other times impairing learning. This review explores the bidirectional effects of estrogens on learning from a multiple memory systems view, focusing on the hippocampus and striatum, whereby modulation by estrogens sorts according to task attributes and neural systems engaged during cognition. We highlight our findings showing that the ability to solve hippocampus-sensitive tasks typically improves under relatively high estrogen status while the ability to solve striatum-sensitive tasks degrades with estrogen exposures. Though constrained by dose and timing of exposure, these opposing enhancements and impairments of cognition can be observed following treatments with different estrogenic compounds including the hormone estradiol, the isoflavone genistein found in soybeans, and agonists that are selective for specific estrogen receptors, suggesting that activation of a single receptor type is sufficient to produce the observed shifts in learning strategies. Using this multi-dimensional framework will allow us to extend our thinking of the relationship between estrogens and cognition to other brain regions and cognitive functions.     

Lateralization in Paridae: comparison of a storing and a non-storing species on a one-trial associative memory task

Summary We present evidence of a difference between a storing and non-storing species in lateralization and transfer of spatial memory processing. Using the technique of monocular occlusion, we compared the performance of a food-storing species, the marsh tit (Parus palustris), with a closely related species that does not store food, the blue tit (P. caeruleus), on a task which relies on one-trial learning for the spatial location of hidden food items. In this one-trial associative learning task, the birds had to return to sites in phase II of a trial where they had been allowed to eat some, but not all, of a piece of peanut in phase I. In the first experiment, in which the birds did not wear eye caps, marsh tits required fewer looks in phase II to find the hidden peanut than blue tits. By categorising the sites as seeded, unseeded or not visited in phase I, further analysis suggested that the two species also differ in the way they behave towards the 3 types of site. Marsh tits appear to distinguish between seeded and other sites, irrespective of whether the other sites were known to be empty (unseeded) or not (not visited); whereas blue tits preferentially returned to those sites that have been visited in phase I, irrespective of whether they contained a seed or not. In the second experiment, all birds wore an eye cap on the left or right eye for phase I and II of each trial. For both species, it was demonstrated that although the visual systems fed by both the right and left eye are involved in short-term storage, the right eye system is associated also with long-term storage. Thus, lateralization was found in both blue tits and marsh tits. However, unilateral transfer of these memories was found only in marsh tits, suggesting that there may be a difference between storers and non-storers in the mechanism of memory processing.     

Brain morphology of the threespine stickleback (Gasterosteus aculeatus) varies inconsistently with respect to habitat complexity: A test of the Clever Foraging Hypothesis

The Clever Foraging Hypothesis asserts that organisms living in a more spatially complex environment will have a greater neurological capacity for cognitive processes related to spatial memory, navigation, and foraging. Because the telencephalon is often associated with spatial memory and navigation tasks, this hypothesis predicts a positive association between telencephalon size and environmental complexity. The association between habitat complexity and brain size has been supported by comparative studies across multiple species but has not been widely studied at the within‐species level. We tested for covariation between environmental complexity and neuroanatomy of threespine stickleback (Gasterosteus aculeatus ) collected from 15 pairs of lakes and their parapatric streams on Vancouver Island. In most pairs, neuroanatomy differed between the adjoining lake and stream populations. However, the magnitude and direction of this difference were inconsistent between watersheds and did not covary strongly with measures of within‐site environmental heterogeneity. Overall, we find weak support for the Clever Foraging Hypothesis in our study.     

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.     

Reptilian Cognition: A More Complex Picture via Integration of Neurological Mechanisms,Behavioral Constraints,and Evolutionary Context

Unlike birds and mammals, reptiles are commonly thought to possess only the most rudimentary means of interacting with their environments, reflexively responding to sensory information to the near exclusion of higher cognitive function. However, reptilian brains, though structurally somewhat different from those of mammals and birds, use many of the same cellular and molecular processes to support complex behaviors in homologous brain regions. Here, the neurological mechanisms supporting reptilian cognition are reviewed, focusing specifically on spatial cognition and the hippocampus. These processes are compared to those seen in mammals and birds within an ecologically and evolutionarily relevant context. By viewing reptilian cognition through an integrative framework, a more robust understanding of reptile cognition is gleaned. Doing so yields a broader view of the evolutionarily conserved molecular and cellular mechanisms that underlie cognitive function and a better understanding of the factors that led to the evolution of complex cognition.     

Why some tits store food and others do not: evaluation of ecological factors

Paridae are among the bird families benefiting from food storing. However, not all its members hoard food. Our objective was to clarify the role of ecological factors in occurrence of food storing. We reviewed the data on major ecological characteristics of the Paridae species and analysed their association with the presence/absence of food storing. Our statistical model revealed that geography (distribution in North America) and taxonomy (genus Poecile) are better predictors of food storing than any of the studied ecological traits. Nevertheless, food-storing Poecile species inhabit mixed or coniferous woodlands with seasonal richness of food, while non-storing species tend to prefer edge and open habitats, where alternative food sources are available. Sociality and territoriality outside breeding season coincides with food storing. The analysis performed within the Baeolophus–Lophophanes–Periparus–Poecile clade with ancestral food storing revealed no factor except continental climate that would explain the persistence of food storing. The phylogenetic analysis of ancestral states of the studied characters allowed us to propose a possible scenario for the emergence of food storing in Paridae. (1) Food storing is not ancestral in Paridae and appeared only once in the common ancestor of the Baeolophus–Lophophanes–Periparus–Poecile group. (2) According to estimation of molecular clock in Paridae, food storing appeared before their radiation in North America.     

Bringing Elton and Grinnell together: a quantitative framework to represent the biogeography of ecological interaction networks

Biogeography has traditionally focused on the spatial distribution and abundance of species. Both are driven by the way species interact with one another, but only recently community ecologists realized the need to document their spatial and temporal variation. Here, we call for an integrated approach, adopting the view that community structure is best represented as a network of ecological interactions, and show how it translates to biogeography questions. We propose that the ecological niche should encompass the effect of the environment on species distribution (the Grinnellian dimension of the niche) and on the ecological interactions among them (the Eltonian dimension). Starting from this concept, we develop a quantitative theory to explain turnover of interactions in space and time – i.e. a novel approach to interaction distribution modeling. We apply this framework to host–parasite interactions across Europe and find that two aspects of the environment (temperature and precipitation) exert a strong imprint on species co‐occurrence, but not on species interactions. Even where species co‐occur, interaction proves to be stochastic rather than deterministic, adding to variation in realized network structure. We also find that a large majority of host‐parasite pairs are never found together, thus precluding any inferences regarding their probability to interact. This first attempt to explain variation of network structure at large spatial scales opens new perspectives at the interface of species distribution modeling and community ecology.