Anat Barnea

Social change affects the survival of new neurons in the forebrain of adult songbirds

Many new neurons are added to the adult avian brain. Most of them die 3-5 weeks after they are born (Nature (Lond.) 335 (1988) 353; J. Comp. Neurol 411 (1999) 487). Those that survive replace, numerically, older ones that have died (Neuron 25 (2000) 481). It has been suggested that the new neurons enhance the brains ability to acquire new long-term memories (review in Sci. Am. 260 (1989) 74). If so, perhaps an increase in social complexity affects the survival of new neurons in a social species. To test this hypothesis, we treated adult zebra finches (Taeniopygia guttata) with [3H]-thymidine immediately before introducing them into one of three different social environments that differed in complexity and killed them 40 days later. There was a significant difference between experimental groups in the number of [3H]-labeled neurons in neostriatum caudale (NC), high vocal center (HVC) and Area X, three forebrain regions that are involved in vocal communication. In these regions, birds placed in a large heterosexual group had more new neurons than birds kept singly or as male-female pairs. Regulation of new neuron survival by extent of circuit use may be a general mechanism for ensuring that neuronal replacement is closely attuned to environmental change.

Birds as a model to study adult neurogenesis: bridging evolutionary, comparative and neuroethological approaches

During the last few decades, evidence has demonstrated that adult neurogenesis is a well‐preserved feature throughout the animal kingdom. In birds, ongoing neuronal addition occurs rather broadly, to a number of brain regions. This review describes adult avian neurogenesis and neuronal recruitment, discusses factors that regulate these processes, and touches upon the question of their genetic control. Several attributes make birds an extremely advantageous model to study neurogenesis. First, song learning exhibits seasonal variation that is associated with seasonal variation in neuronal turnover in some song control brain nuclei, which seems to be regulated via adult neurogenesis. Second, food‐caching birds naturally use memory‐dependent behavior in learning the locations of thousands of food caches scattered over their home ranges. In comparison with other birds, food‐caching species have relatively enlarged hippocampi with more neurons and intense neurogenesis, which appears to be related to spatial learning. Finally, migratory behavior and naturally occurring social systems in birds also provide opportunities to investigate neurogenesis. This diversity of naturally occurring memory‐based behaviors, combined with the fact that birds can be studied both in the wild and in the laboratory, make them ideal for investigation of neural processes underlying learning. This can be done by using various approaches, from evolutionary and comparative to neuroethological and molecular. Finally, we connect the avian arena to a broader view by providing a brief comparative and evolutionary overview of adult neurogenesis and by discussing the possible functional role of the new neurons. We conclude by indicating future directions and possible medical applications.

What parts of fleshy fruits contain secondary compounds toxic to birds and why.

Abstract Saponins, flavonoids and cyanogenic glycosides were surveyed in pulps and seeds of wild, bird-dispersed fleshy fruits of hawthorn ( Crataegus monogyna ), ivy ( Hedera helix ), holly ( Ilex aquifolium ), and yew ( Taxus baccata ). Interactions between three of the four species (hawthorn, holly, and yew) and their avian seed dispersers were studied in the field. The results indicate that when different bird species foraged on the same fruit they spend similar periods of time on the tree and eat a similar number of fruits at each feeding bout. Frugivorous birds stayed on all plant species for short periods of time (1.3–5.3 min) and consumed only a few fruits in each feeding bout (4.3–6.5 min). There is a differential occurrence of secondary compounds in fruit parts: in most cases allelochemicals were found in pulps but not seeds. These findings confirm the hypothesis that mild toxicity in the pulp can prevent consumption of too many fruits in one foraging bout and regulate seed retention time. This, combined with the short visits ensures better seed dispersal, as only few seeds will be deposited in one site at one time. Yew presents a special case, since cyanogenic glycosides were identified only in seed-coats, while both the fleshy aril and seed content are free of this toxin. A possible ecological explanation is suggested for this finding. The concentrations of some compounds may change during fruit ripening.

Social and spatial changes induce multiple survival regimes for new neurons in two regions of the adult brain: An anatomical representation of time?

Male zebra finches reared in family groups were housed initially in small indoors cages with three other companions. At 4-5 months of age these birds were treated with [(3)H]-thymidine and then placed in large outdoors aviaries by themselves or with other zebra finches. Counts of new neurons were made 40, 60 and 150 days after the change in housing. Recruitment of new neurons in nidopallium caudale (NC) was higher than in the hippocampal complex (HC); but in both brain regions it was higher in communally housed birds than in birds housed singly, suggesting that the complexity of the social setting affects new neuron survival. In addition, the new neurons lived longer in rostral NC than in its caudal counterpart, and neuronal turnover was faster and more significant in NC than in HC. Albeit indirect, this may be the first suggestion that different parts of the brain upgrade memories at different time intervals, yielding an anatomical representation of time.

Better than sleep: theta neurofeedback training accelerates memory consolidation.

Consistent empirical results showed that both night and day sleep enhanced memory consolidation. In this study we explore processes of consolidation of memory during awake hours. Since theta oscillations have been shown to play a central role in exchange of information, we hypothesized that elevated theta during awake hours will enhance memory consolidation. We used a neurofeedback protocol, to enhance the relative power of theta or beta oscillations. Participants trained on a tapping task, were divided into three groups: neurofeedback theta; neurofeedback beta; control. We found a significant improvement in performance in the theta group, relative to the beta and control groups, immediately after neurofeedback. Performance was further improved after night sleep in all groups, with a significant advantage favoring the theta group. Theta power during training was correlated with the level of improvement, indicating a clear relationship between memory consolidation, and theta neurofeedback.

The relationship between nature of social change, age, and position of new neurons and their survival in adult zebra finch brain.

Some kinds of neurons are spontaneously recruited in the intact, healthy adult brain, but the variables that affect their survival are not always clear. We show that in caudal nidopallium of adult male zebra finches, the rostrocaudal position of newly recruited neurons, their age (1 vs 3 months), and the nature of social change (complex vs simple) after the neurons were born affect their survival. Greater social complexity promoted the survival of younger new neurons, and the demise of older ones; a less marked social change promoted the survival of older new neurons. These effects were position dependent. We suggest that functional correlations between new neuron recruitment/survival and its inferred benefit to the animal might be better perceived when taking into account the position of cells, their age at the time of life style changes, and the nature and magnitude of the life style change.

The effect of social environment on singing behavior in the zebra finch (Taeniopygia guttata) and its implication for neuronal recruitment

Previous studies found that complex social environment increases new neuronal recruitment in brains of adult male zebra finches, in comparison with exposure to a simple social environment. These experiments could not determine, however, whether this increase was due to greater amounts of auditory input (amount of auditory information the male is exposed to), or auditory output (amount of song it produces). To answer this question, we raised male zebra finches to adulthood in a controlled environment, and were then exposed them to either a single unfamiliar female (simple social environment) or to 45 unfamiliar zebra finches of both sexes (complex social environment). Their singing behavior was monitored in these new social environments. Birds which were exposed to a simple social environment sang significantly more than birds which were exposed to a complex social environment. This supports the hypothesis that increased neuronal recruitment in birds exposed to a complex social environment correlates with processing and storing of auditory input, and not with song produced by the bird.

Selective loss of glycogen synthase kinase-3α in birds reveals distinct roles for GSK-3 isozymes in tau phosphorylation

Mammalian glycogen synthase kinase‐3 (GSK‐3), a critical regulator in neuronal signaling, cognition, and behavior, exists as two isozymes GSK‐3α and GSK‐3β. Their distinct biological functions remains largely unknown. Here, we examined the evolutionary significance of each of these isozymes. Surprisingly, we found that unlike other vertebrates that harbor both GSK‐3 genes, the GSK‐3α gene is missing in birds. GSK‐3‐mediated tau phosphorylation was significantly lower in adult bird brains than in mouse brains, a phenomenon that was reproduced in GSK‐3α knockout mouse brains. Tau phosphorylation was detected in brains from bird embryos suggesting that GSK‐3 isozymes play distinct roles in tau phosphorylation during development. Birds are natural GSK‐3α knockout organisms and may serve as a novel model to study the distinct functions of GSK‐3 isozymes.

Frequent summer nuptial flights of ants provide a primary food source for bats

In many ant species, nuptial flight tends to be short in time and assumed to be synchronous across a large area. Here, we report that, in the upper Jordan Valley, northern Israel, massive nuptial flights of Carpenter ants (Camponotus sp.) occur frequently throughout the summer, and their alates form up to 90% of the diet of the greater mouse-tailed bat (Rhinopoma microphyllum) during this period. This fat and protein-rich diet enables female bats to lactate during summer, and the large amount of fat that both sexes accumulate may serve as an energy source for their following winter hibernation and posthibernation mating in early spring (March–April). We suggest that the annual movement of these bats to the Mediterranean region of Israel may have evolved in order to enable them to exploit the extremely nutritious forms of ant alates when the bats’ energetic demands are highest.

Interactions between environmental changes and brain plasticity in birds.

Neurogenesis and neuronal recruitment occur in many vertebrates, including humans. Most of the new neurons die before reaching their destination. Those which survive migrate to various brain regions, replace older ones and connect to existing circuits. Evidence suggests that this replacement is related to acquisition of new information. Therefore, neuronal replacement can be seen as a form of brain plasticity that enables organisms to adjust to environmental changes. However, direct evidence of a causal link between replacement and learning remains elusive. Our hypothesis is that increased neuronal recruitment is associated with increase in memory load. Moreover, since neuronal recruitment is part of a turnover process, we assume that the same conditions that favor survival of some neurons induce the death of others. I present studies that investigated the effect of various behaviors and environmental conditions (food-hoarding, social change, reproductive cycle) on neuronal recruitment and survival in adult avian brains, and discuss how these phenomena relate to the life of animals. I offer a frame and rationale for comparing neuronal replacement in the adult brain, in order to uncover the pressures, rules, and mechanisms that govern its constant rejuvenation. The review emphasizes the importance of using various approaches (behavioral, anatomical, cellular and hormonal) in neuroethological research, and the need to study natural populations, in order to fully understand how neurogenesis and neuronal replacement contribute to life of animals. Finally, the review indicates to future directions and ends with the hope that a better understanding of adult neuronal replacement will lead to medical applications.