Memory and the hippocampus in food-storing birds: a comparative approach

Comparative studies provide a unique source of evidence for the role of the hippocampus in learning and memory. Within birds and mammals, the hippocampal volume of scatter-hoarding species that cache food in many different locations is enlarged, relative to the remainder of the telencephalon, when compared with than that of species which cache food in one larder, or do not cache at all. Do food-storing species show enhanced memory function in association with the volumetric enlargement of the hippocampus? Comparative studies within the parids (titmice and chickadees) and corvids (jays, nutcrackers and magpies), two families of birds which show natural variation in food-storing behavior, suggest that there may be two kinds of memory specialization associated with scatter-hoarding. First, in terms of spatial memory, several scatter-hoarding species have a more accurate and enduring spatial memory, and a preference to rely more heavily upon spatial cues, than that of closely related species which store less food, or none at all. Second, some scatter-hoarding parids and corvids are also more resistant to memory interference. While the most critical component about a cache site may be its spatial location, there is mounting evidence that food-storing birds remember additional information about the contents and status of cache sites. What is the underlying neural mechanism by which the hippocampus learns and remembers cache sites? The current mammalian dogma is that the neural mechanisms of learning and memory are achieved primarily by variations in synaptic number and efficacy. Recent work on the concomitant development of food-storing, memory and the avian hippocampus illustrates that the avian hippocampus may swell or shrivel by as much as 30% in response to presence or absence of food-storing experience. Memory for food caches triggers a dramatic increase in the total number of number of neurons within the avian hippocampus by altering the rate at which these cells are born and die.     

What food-storing birds remember.

A synthesis of previous studies suggests that food-storing birds are able to remember the spatial locations of large numbers of scattered caches for periods ranging from a few days to several months and use visual cues to do so. The birds can perform a number of operations on the remembered set of storage sites, including recalling which caches have been previously exploited and which have been lost to other animals. The behavior of food-storing birds is compared with that of other animals in laboratory studies of memory with respect to the number of items that can be recalled, the length of retention intervals, and serial-position effects. (French abstract) (62 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Imprinting, learning and development: from behaviour to brain and back

Neural and behavioural analyses have shown that the formation of filial preferences in young, precocial birds involves at least two separate processes. One process is an emerging predisposition to approach stimuli with the characteristics of the natural mother. The other (learning) process of filial imprinting results in chicks preferentially-approaching a stimulus to which they have been exposed and involves forming links between the components of the exposed stimulus. The neural substrate for the predisposition is different from that underlying imprinting, and different regions of the chick brain are involved in distinct aspects of learning about imprinting stimuli.     

Visual lateralization in birds: from neurotrophins to cognition?

Birds which are tested monocularly in visual discrimination tasks generally show higher performance levels with the right eye seeing. Due to the virtual complete decussation of the optic nerves, a right eye superiority is probably related to a left hemisphere dominance. If visual processes between the hemispheres differ, each half-brain might be differently prone to be deceived by visual illusions. Indeed pigeons tested with the herringbone illusions are deceived to a stronger extent with the right eye. These functional asymmetries are accompanied by anatomical left-right differences in the ascending thalamo- and tectofugal visual pathways in chicks and pigeons, respectively. The neuroanatomical and behavioral assymmetries result from an asymmetrical posture before hatching in which the embryo keeps his head turned to the right, such that the right eye is stimulated by light shining through the shell. The lateralization of adult animals are induced by this prehatching asymmetric photic stimulation since dark incubation abolishes behavioral and anatomical asymmetries. It is conceivable that the asymmetrical embryonal light stimulation increases the release of neurotrophins in the developing avian visual system in an activity dependent matter. Neurotrophins play an important role in neuronal survival and morphology and thus might represent a molecular switch bridging the gap from embryonal light stimulation to asymmetries of visual cognition in adults.     

Memory in the chick: Multiple cues, distinct brain locations.

Training chicks on a 1-trial passive avoidance task results in memory-dependent synaptic remodeling in the intermediate medial hyperstriatum ventrale (IMHV) and lobus parolfactorius (LPO). Because pretraining IMHV lesions are amnestic and posttraining IMHV lesions are not, the functional significance of this remodeling requires explanation. Chicks use various cues to classify and remember objects. If the IMHV were concerned with memory for only one such cue, then posttraining IMHV lesions would not lead to "amnesia" because animals would still avoid the aversive bead using other contextual cues. This hypothesis was tested using a color discrimination task. IMHV lesions, but not LPO lesions, impair color discrimination, suggesting that the IMHV may be involved in classifying and remembering the bitter bead on the basis of color. Thus, even simple associations are stored in the brain in the form of multiple, dispersed representations. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Memory and the brain: unexpected chemistries and a new pharmacology

Efforts to characterize long-term potentiation (LTP) and to identify its substrates have led to the discovery of novel synaptic chemistries, computational algorithms, and, most recently, pharmacologies. Progress has also been made in using LTP to develop a "standard model" of how unusual, but physiologically plausible, levels of afferent activity create lasting changes in the operating characteristics of synapses in the cortical telencephalon. Hypotheses of this type typically distinguish induction, expression, and consolidation stages in the formation of LTP. Induction involves a sequence consisting of theta-type rhythmic activity, suppression of inhibitory currents, intense synaptic depolarization, NMDA receptor activation, and calcium influx into dendritic spines. Calcium-dependent lipases, kinases, and proteases have been implicated in LTP induction. Regarding the last group, it has been recently reported that theta pattern stimulation activates calpain and that translational suppression of the protease blocks potentiation. It is thus likely that proteolysis is readily driven by synaptic activity and contributes to structural reorganization. LTP does not interact with treatments that affect transmitter release, has a markedly differential effect on the currents mediated by colocalized AMPA vs NMDA synaptic receptors, changes the waveform of the synaptic current, modifies the effects of drugs that modulate AMPA receptors, and is sensitive to the subunit composition of those receptors. These results indicate that LTP is expressed by changes in AMPA receptor operations. LTP is accompanied by modifications in the anatomy of synapses and spines, something which accounts for its extreme duration (weeks). As with various types of memory, LTP requires about 30 min to consolidate (become resistant to disruption). Consolidation involves adhesion chemistries and, in particular, activation of integrins, a class of transmembrane receptors that control morphology in numerous cell types. Platelet activating factor and adenosine may contribute to consolidation by regulating the engagement of latent integrins. How consolidation stabilizes LTP expression is a topic of intense investigation but probably involves modifications to one or more of the following: membrane environment of AMPA receptors; access of regulatory proteins (e.g., kinases, proteases) to the receptors; receptor clustering; and space available for receptor insertion. Attempts to enhance LTP have focused on the induction phase and resulted in a class of centrally active drugs ("ampakines") that positively modulate AMPA receptors. These compounds promote LTP in vivo and improve the encoding of variety of memory types in animals. Positive results have also been obtained in preliminary studies with humans.     

Memory stages and brain asymmetry in chick learning.

Stages of formation of memory and the roles of different forebrain structures in memory formation were investigated by injecting various agents into the brains of chicks close to the time of peck-avoidance training. With L-glutamate injected bilaterally into the hyperstriatum 5 min pretraining, retention was good 1 min posttraining but significantly impaired at 5 min and each subsequent time point from 10 min to 24 hr. With ouabain, retention declined more slowly, showing significant impairment at 15 min and thereafter. With any of 3 protein synthesis inhibitors, retention was still good 60 min posttraining but significantly impaired at 90 min. The 3 time courses of decline of retention are consistent with hypotheses of 3 sequentially dependent stages of memory formation. It appears that both the medial hyperstriatum and the lateral neostriatum are required for formation of memory. Agents that are specific for a presumed stage of memory formation and whose action is restricted spatially should help reveal the roles of different brain structures in different stages of memory formation. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Mammalian sex determination: from gonads to brain

In mammals, sex is determined by the Y chromosome, which encodes a testis-determining factor (TDF). This factor causes the undifferentiated embryonic gonads to develop as testes rather than ovaries. The testes subsequently produce the male sex hormones that are responsible for all male sexual characteristics. In 1990, the sex-determining gene, TDF, was identified and termed SRY in humans (Sry in mice). It encodes a protein containing a high mobility group (HMG) motif, which confers the ability to bind and to bend DNA. Genetic evidence supporting SRY as TDF came from the observation of a male phenotype in XX mice transgenic for a small genomic fragment containing Sry, and from the study of XY sex-reversed individuals who harbor de novo mutations in the SRY coding sequence. Other non-Y-linked genes involved in sex determination were subsequently found by genetic analysis of XY sex-reversed patients not explained by mutations in SRY. These genes are WT1, SF1, DAX1, and SOX9. A regulatory cascade hypothesis for mammalian sex determination, proposing that SRY represses a negative regulator of male development, was recently supported by observation of mice that expressed a DAX1 transgene and developed as XY sex-reversed females. The role of some sex-determining genes, such as DAX1 and SF1, in the development of the entire reproductive axis, a functionally integrated endocrine axis, leads to a new concept. Normal sexual development may result from the functional and developmental integration of a number of different genes that play roles in sex determination, sexual differentiation, and sexual behavior.     

Memory systems in the brain and localization of a memory

It is now clear that there are a number of different forms or aspects of learning and memory that involve different brain systems. Broadly, memory phenomena have been categorized as explicit or implicit. Thus, explicit memories for experience involve the hippocampus-medial temporal lobe system and implicit basic associative learning and memory involves the cerebellum, amygdala, and other systems. Under normal conditions, however, many of these brain-memory systems are engaged to some degree in learning situations. But each of these brain systems is learning something different about the situation. The cerebellum is necessary for classical conditioning of discrete behavioral responses (eyeblink, limb flexion) under all conditions; however, in the "trace" procedure where a period of no stimuli intervenes between the conditioned stimulus and the unconditioned stimulus the hippocampus plays a critical role. Trace conditioning appears to provide a simple model of explicit memory where analysis of brain substrates is feasible. Analysis of the role of the cerebellum in basic delay conditioning (stimuli overlap) indicates that the memories are formed and stored in the cerebellum. The phenomenon of cerebellar long-term depression is considered as a putative mechanism of memory storage.     

Neuronal regeneration: extending axons from bench to brain

Many studies have shown that myelin in the central nervous system strongly inhibits the regeneration of axons, so it comes as a surprise to discover that adult neurons transplanted into the brain rapidly extend their axons through myelinated pathways.     

The vesicular monoamine transporter: from chromaffin granule to brain

All characterized monoaminergic cells utilize the same transport system for the vesicular accumulation of monoamines prior to their release. This system operates in neuronal (catecholaminergic, serotoninergic or histaminergic) as well as in endocrine or neuroendocrine cells. For several decades, chromaffin granules from bovine adrenal medulla have been used as a model system, allowing progress in the understanding of the biophysics, the biochemistry and the pharmacology of the monoamine vesicular transporter. The transporters from rat, bovine and man have been cloned. Surprisingly, two genes encode different isoforms of the protein which are differentially expressed in monoaminergic systems. The conjunction of recombinant DNA techniques and expression in secretory or non-secretory cells with the large body of data obtained on the chromaffin granule transporter has allowed rapid progress in the study of the protein. But interestingly enough, this progress has open new possibilities in the study of biological problems, especially in the brain. The transporter is useful for the determination of the relationship between small and large dense core vesicles, for the understanding of the mechanism of the drugs such as 1-methyl-4-phenylpyridinium (MPP+), tetrabenazine or amphetamines, and as a marker in brain development. The possibility of regulations at the vesicular transporter level and of their effect on the quantum size has to be investigated. The vesicular monoamine transporter is also an important target for brain imaging.     

Social and hormonal bases of individual differences in the parental behaviour of birds and mammals.

We present an overview of research on how social experiences and hormonal responses affect individual variation in parental care of birds and mammals. The parental roles of prolactin and glucorticoids (corticosterone or cortisol) have many similarities in birds and in mammals. Prolactin may be involved in the initiation of parental interactions, with prolactin variation possibly explaining individual differences in parental decision-making. Glucocorticoid levels increase when parents have to work harder, with some individuals showing greater hormonal and behavioural responses than others. Testosterone interferes with paternal behaviour in birds, but its role is more complex and species-specific in male mammals. We examine these differences in an adaptive framework, where retaining flexibility of response has allowed individuals to respond differentially to social opportunities and environmental change. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Blood parasites in birds from Monteverde, Costa Rica

In a survey of avian blood parasites in Costa Rica, 51 (11%) of 479 birds sampled were infected by at least one species of hematozoan. Fourteen of the 60 species of birds in the survey were examined for the first time. Infections were most common in ramphastids and emberizids and infrequent in other taxa. Among resident species, infections were more commonly detected during the wet season when most birds breed than during the dry season when few birds breed. Infections caused by Haemoproteus sp. were most common, while Plasmodium sp., Leucocytozoon sp., Trypanosoma sp., and microfilarial infections were rare. The intensity of the 40 Haemoproteus infections in adult birds was low, with a mean +/- SE of 12.5 +/- 3.7 infected cells per 10,000. Haemoproteus infections did not undergo seasonal changes in intensity.     

Verbal and Visual Memory Index discrepancies from the Wechsler Memory Scale—Revised: Cautions in interpretation.

The present study examined the clinical utility of the Wechsler Memory Scale—Revised (WMS—R; D. Wechsler, 1987) Verbal and Visual Memory Indexes to predict laterality of previous temporal lobectomy (TL) in 13 left (L; 7 men, 5 women) and 20 right (R; 11 men, 9 women) patients. Three verbal–visual index discrepancy criteria were used. Of the 16 patients with difference scores of at least 16 points (least conservative criterion), 9 had index discrepancies that incorrectly identified resection laterality (i.e., Verbal Memory Index decreased relative to Visual Memory Index in RTL patients). Five of 11 patients with index discrepancies of 21 or more points were incorrectly classified. Only 1 of 4 patients was incorrectly classified using a 29-point discrepancy criterion, although 2 RTL patients had discrepancy scores of 28 points in the incorrect direction. Consequently, users of the WMS—R are cautioned against inferring laterality of lesion on the basis of the Verbal and Visual Memory Indexes alone. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Hippocampus and memory in a food-storing and in a nonstoring bird species.

Food-storing birds maintain in memory a large and constantly changing catalog of the locations of stored food. The hippocampus of food-storing black-capped chickadees (Panus atricapillus) is proportionally larger than that of nonstoring dark-eyed juncos (Junco hyemalis). Chickadees perform better than do juncos in an operant test of spatial non-matching-to-sample (SNMTS), and chickadees are more resistant to interference in this paradigm. Hippocampal lesions attenuate performance in SNMTS and increase interference. In tests of continuous spatial alternation (CSA), juncos perform better than chickadees. CSA performance also declines following hippocampal lesions. By itself, sensitivity of a given task to hippocampal damage does not predict the direction of memory differences between storing and nonstoring species. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Avian polymavirus in wild birds: genome analysis of isolates from Falconiformes and Psittaciformes

Avian polyomavirus (APV) infections have been reported to cause fatal disease in a wide range of psittacine species. Here we demonstrate APV infections in buzzards (Buteo buteo) and in a falcon (Falco tinnunculus) found dead in Germany, and in lovebirds (Agapornis pullaria) with fatal disease, wild-caught in Mo?ambique. APV infection in buzzards was determined by PCR amplification of parts of the viral genome followed by Southern blot hybridisation. The genomes of the isolates obtained from the falcon and one of the lovebirds proved to be very closely related to those of Budgerigar Fledgling Disease Virus (BFDV)-1, BFDV-2 and BFDV-3, isolated from budgerigar, chicken, and parakeet, respectively. A consensus sequence was delineated from the known nucleotide sequences of APV isolates. The significance of some nucleotide changes is discussed. Infectivity of all of these isolates was neutralized by antibodies directed against BFDV-1. Data presented in this investigation show that the polyomavirus isolates obtained from different avian species so far all belong to one genotype and one serotype within the proposed subgenus Avipolyomavirus of the family Papovaviridae. The designation Budgerigar Fledgling Disease Virus (BFDV) is, therefore, misleading as this virus type infects different species of birds. The name Avian Polymavirus and the abreviation APV should be adopted to all of the isolates investigated in detail at present. The possible role of birds of passage in the epidemiology in APV infections is discussed.     

Divided attention, memory, and spatial discrimination in food-storing and nonstoring birds, black-capped chickadees ( Poecile atricapilla) and dark-eyed Juncos ( Junco hyemalis).

Food-storing birds, black-capped chickadees (Poecile atricapilla), and nonstoring birds, dark-eyed juncos (Junco hyemalis), matched color or location on a touch screen. Both species showed a divided attention effect for color but not for location (Experiment 1). Chickadees performed better on location than on color with retention intervals up to 40 s, but juncos did not (Experiment 2). Increasing sample-distractor distance improved performance similarly in both species. Multidimensional scaling revealed that both use a Euclidean metric of spatial similarity (Experiment 3). When choosing between the location and color of a remembered item, food storers choose location more than do nonstorers. These results explain this effect by differences in memory for location relative to color, not division of attention or spatial discrimination ability. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Development of object permanence in food-storing magpies (Pica pica).

The development of object permanence was investigated in black-billed magpies (Pica pica), a food-storing passerine bird. The authors tested the hypothesis that food-storing development should be correlated with object-permanence development and that specific stages of object permanence should be achieved before magpies become independent. As predicted, Piagetian Stages 4 and 5 were reached before independence was achieved, and the ability to represent a fully hidden object (Piagetian Stage 4) emerged by the age when magpies begin to retrieve food. Contrary to psittacine birds and humans, but as in dogs and cats, no "A-not-B error" occurred. Although magpies also mastered 5 of 6 invisible displacement tasks, evidence of Piagetian Stage 6 competence is ambiguous. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Progress in the study of brain evolution: from speculative theories to testable hypotheses

Darwin's theory of evolution raised the question of how the human brain differs from that of other animals and how it is the same. Early students of brain evolution had constructed rather grand but speculative theories which stated that brains evolved in a linear manner, from fish to man and from simple to complex. These speculations were soundly refuted, however, as contemporary comparative neurobiologists used powerful new techniques and methodologies to discover that complex brains have evolved several times independently among vertebrates (e.g., within teleost fishes and birds) and that brain complexity has actually decreased in the lineages leading to modern salamanders and lungfishes. Moreover, the old idea that brains evolved by the sequential addition of new components has now been replaced by the working hypothesis that brains generally evolve by the divergent modification of preexisting parts. Speculative theories have thus been replaced by testable hypotheses, and current efforts in the field are aimed at making phylogenetic hypotheses even more testable. Particularly promising new directions for comparative neurobiology include (1) the integration of comparative neuroanatomy with comparative embryology and developmental genetics in order to test phylogenetic hypotheses at a mechanistic level, (2) research into how evolutionary changes in the structure of neural circuits are related to evolutionary changes in circuit function and animal behavior, and (3) the analysis of independently evolved similarities to discover general rules about how brains may or may not change during the course of evolution.