Experience-Expectant Plasticity in the Mushroom Bodies of the Honeybee

Worker honeybees (Apis mellifera) were reared in social isolation in complete darkness to assess the effects of experience on growth of the neuropil of the mushroom bodies (MBs) during adult life. Comparison of the volume of the MBs of 1-day-old and 7-day-old bees showed that a significant increase in volume in the MB neuropil occurred during the first week of life in bees reared under these highly deprived conditions. All regions of the MB neuropil experienced a significant increase in volume with the exception of the basal ring. Measurement of titers of juvenile hormone (JH) in a subset of bees indicated that, as in previous studies, these rearing conditions induced in some bees the endocrine state of high JH associated with foraging, but there was no correlation between JH titer and volume of MB neuropil. Treatment of another subset of dark-reared bees with the JH analog, methoprene, also had no effect of the growth of the MB neuropil. These results demonstrate that there is a phase of MB neuropil growth early in the adult life of bees that occurs independent of light or any form of social interaction. Together with previous findings showing that an increase in MB neuropil volume begins around the time that orientation flights occur and then continues throughout the phase of life devoted to foraging, these results suggest that growth of the MB neuropil in adult bees may have both experience-expectant and experience-dependent components.     

Repeated cocaine experience facilitates sucrose-reinforced operant responding in enriched and isolated rats

The purpose of the present experiment was to determine whether repeated cocaine exposure differentially affects sucrose-reinforced operant responding in rats raised in an enriched condition (EC) or an isolated condition (IC). Specifically, the performance of EC and IC rats pressing a lever for sucrose under a high fixed-ratio schedule (FR 30) prior to and after 10 days of exposure to cocaine (15 mg/kg, i.p.) or saline was compared. Regardless of rearing condition, rats repeatedly exposed to cocaine had shorter reacquisition latencies to complete a sucrose-reinforced FR 30 task than saline controls. The results suggest that cocaine exposure may have cross-sensitized both EC and IC rats to the reinforcing effects of sucrose or sucrose-associated cues, thus facilitating reacquisition of operant responding.     

Integrative Properties of the Pe1 Neuron, a Unique Mushroom Body Output Neuron

A mushroom body extrinsic neuron, the Pe1 neuron, connects the peduncle of the mushroom body (MB) with two areas of the protocerebrum in the honeybee brain, the lateral protocerebral lobe (LPL) and the ring neuropil around the α-lobe. Each side of the bee brain contains only one Pe1 neuron. Using a combination of intracellular recording and neuroanatomical techniques we analyzed its properties of integrative processing of the different sensory modalities. The Pe1 neuron responds to visual, mechanosensory, and olfactory stimuli. The responses are broadly tuned, consisting of a sustained increase of spike frequency to the onset and offset of light flashes, to horizontal and vertical movements of extended objects, to mechanical stimuli applied to the antennae or mouth parts, and to all olfactory stimuli tested (29 chemicals). These multisensory properties are reflected in its dendritic organization. Serial reconstructions of intracellularly stained Pe1 neurons using confocal microscopy reveal that the Pe1 neuron arborizes throughout all layers of MB peduncle with finger-like, vertically oriented dendrites. The peduncle of the MB is formed by the axons of Kenyon cells, whose dendritic inputs are organized in modality-specific subcompartments of the calyx region. The peduncular arborization indicates that the Pe1 neuron receives input from Kenyon cells of all calycal subcompartments. Because the Pe1 neuron changes its odor responses transiently as a consequence of olfactory learning, we hypothesize that the multimodal response properties might have a role in memory consolidation and help to establish contextual references in the long-term trace.     

Exploration of virtual mazes by rhesus monkeys (<Emphasis Type="Italic">Macaca mulatta</Emphasis>)

A chasm divides the huge corpus of maze studies found in the literature, with animals tested in mazes on the one side and humans tested with mazes on the other. Advances in technology and software have made possible the production and use of virtual mazes, which allow humans to navigate computerized environments and thus for humans and nonhuman animals to be tested in comparable spatial domains. In the present experiment, this comparability is extended even further by examining whether rhesus monkeys (Macaca mulatta) can learn to explore virtual mazes. Four male macaques were trained to manipulate a joystick so as to move through a virtual environment and to locate a computer-generated target. The animals succeeded in learning this task, and located the target even when it was located in novel alleys. The search pattern within the maze for these animals resembled the pattern of maze navigation observed for monkeys that were tested on more traditional two-dimensional computerized mazes.     

Early Development of Mushroom Bodies in the Brain of the Honeybee Apis mellifera as Revealed by BrdU Incorporation and Ablation Experiments

In the honeybee the mushroom bodies are prominent neuropil structures arranged as pairs in the dorsal protocerebrum of the brain. Each mushroom body is composed of a medial and a lateral subunit. To understand their development, the proliferation pattern of mushroom body intrinsic cells, the Kenyon cells, were examined during larval and pupal stages using the bromodeoxyuridine (BrdU) technique and chemical ablation with hydroxyurea.     

Behavioral responses of juvenile rats (Rattus norvegicus) to neonates after infusion of maternal blood plasma

Individual 18- or 30-day-old male and female Wistar rats (juveniles) were continuously exposed to 3-8-day-old pups for 5 days (sensitization) after intravenous (iv) infusion of maternal blood plasma (PL group) or 5% dextrose and water (IC group) through chronically implanted cannulas and were compared with nonhandled littermate controls (NHC group). The results showed complex interactions with sex and age of the animals tested, depending upon which maternal behaviors were examined. First, plasma from parturient females selectively increased retrieving behavior in 30-day-olds, and it was more powerful in females than in males. Second, on the first day, prior to sensitization, both PL and IC 30-day-olds showed higher frequencies of retrieving, crouching, anogenital licking, and contact than did nonhandled juveniles. Third, 30-day-olds that received maternal blood plasma continued to retrieve pups, with a latency peak for retrieving occurring at 72 hours, suggesting a long-term effect of plasma not seen in control animals. Fourth, 18-day-old subjects did not generally show effects of any of our manipulations, but they did show more nest building and contact behaviors than did 30-day-old subjects. Last, we found that the iv cannulation and infusion procedures led to a persistent dissociation of retrieving behavior from play in older animals and an integration of retrieving with crouching and licking regardless of whether maternal plasma or control infusion was administered. Retrieving behavior was associated with play behaviors (charge and pounce) in younger juveniles and in older, nonhandled control animals irrespective of treatment. For these animals, no integration of retrieving occurred with other maternal behaviors.     

Spatial cognition in zebrafish: the role of strain and rearing environment

Two strains of zebrafish, WIK and a second-generation wild strain were reared in either a structurally simple or complex environment and compared in their ability to locate a food reward in a five-chambered maze. There was a significant interaction within subjects between rearing environment and trial, indicating that the consistency of learning varied depending on rearing environment, with those reared in a structurally simple environment showing a slower rate of learning. Fish of both strains reared in a structurally complex environment were smaller than those reared in a simple environment. Our study demonstrates, for the first time in zebrafish, that performance in a learning task as an adult is sensitive to rearing conditions during development.     

Behavioural inhibition and the age at social isolation in rats

Rats that were socially isolated or group-housed at weaning were re-housed at 51 days of age in either the same housing condition or the opposite housing condition until 91 days and throughout subsequent behavioural testing. Increased resistance to extinction of running in an alley and poorer Hebb-Williams maze learning were found only after social isolation between 23 and 51 days of age. In contrast, slower running to reach the water reward during alley training and lower rearing activity at the beginning of open field testing were evident only in rats that were isolated at the time of testing. As in previous studies, open field hyperactivity was found in rats isolated at weaning but slower emergence latency was found in animals isolated at the time of testing. These findings confirm that the many behavioural effects of social isolation at different ages do not reflect a unitary aetiology. The behaviour of rats isolated at weaning is suggestive of a “disinhibition syndrome” but the precise nature of this syndrome is as yet unclear.     

The effects of p-chloroamphetamine, a depletor of brain serotonin, on the performance of rats in two types of positively reinforced complex spatial discrimination tasks

Learning in male Sprague-Dawley rats was assessed in two types of positively reinforced complex spatial discrimination tasks (Stone 14-unit T-maze and eight-arm radial-arm maze) following cytotoxic lesions of central serotonergic terminal projection fields with p-chloroamphetamine (PCA). Learning, as expressed as mean number of errors per day and mean number of trails required to reach criterion, was significantly enhanced in the PCA-lesioned animals trained in the Stone maze. On the other hand, the performance of the PCA-lesioned animals trained in the eight-arm radial-arm maze was not found to differ significantly from that of saline-injected animals. The improved acquisition of the PCA-lesioned rats trained in the Stone maze was completely abolished following pretreatment with the selective serotonergic reuptake inhibitor norzimeldine. Neurochemical analyses of the brains of representative animals revealed that the levels of serotonin and its major metabolite, 5-hydroxy-3-indoleacetic acid, were both significantly reduced by PCA in all regions examined. While it is clear from these and other studies that the serotonergic nervous system plays an important role in the processes underlying learning and memory, these results further underscore the selective role of this neurotransmitter system in the way information is processed by the brain.     

Cognition and Emotion,Volume 24, 2010, List of Reviewers

The tendency for anxious individuals to selectively attend to threatening information is believed to cause and exacerbate anxious emotional responding in a self-perpetuating cycle. The present study sought to examine the relation between differential interoceptive conditioning (IC) using carbon dioxide inhalation as a panicogenic unconditioned stimulus (US) and the development of Stroop colour-naming interference to various non-word conditioned stimuli (CSs). Healthy university students (N = 27) underwent the assessment of colour-naming interference to reinforced CS+ and non-reinforced CS? non-words prior to and following differential fear conditioning. Participants showed greater magnitude electrodermal and verbal-evaluative responses to the CS+ over the CS? non-word following IC, and demonstrated the expected slower colour-naming latencies to the CS+ compared to the CS? non-word from baseline to post-conditioning. We discuss the relation between fear learning and the emergence of attentional bias for threat to further understand the maintenance of anxiety disorders.     

Different early rearing experiences have long‐term effects on cortical organization in captive chimpanzees (Pan troglodytes)

Consequences of rearing history in chimpanzees (Pan troglodytes) have been explored in relation to behavioral abnormalities and cognition; however, little is known about the effects of rearing conditions on anatomical brain development. Human studies have revealed that experiences of maltreatment and neglect during infancy and childhood can have detrimental effects on brain development and cognition. In this study, we evaluated the effects of early rearing experience on brain morphology in 92 captive chimpanzees (ages 11–43) who were either reared by their mothers (n = 46) or in a nursery (n = 46) with age‐group peers. Magnetic resonance brain images were analyzed with a processing program (BrainVISA) that extracts cortical sulci. We obtained various measurements from 11 sulci located throughout the brain, as well as whole brain gyrification and white and grey matter volumes. We found that mother‐reared chimpanzees have greater global white‐to‐grey matter volume, more cortical folding and thinner grey matter within the cortical folds than nursery‐reared animals. The findings reported here are the first to demonstrate that differences in early rearing conditions have significant consequences on brain morphology in chimpanzees and suggests potential differences in the development of white matter expansion and myelination.     

Maternal aggression in mice: The non-specific nature of the exteroceptive maintenance by young

Five hours of pup removal during early lactation (Postpartum Day 6) reduced maternal aggression in mice, while placement of the dam's entire litter (six pups) or a single pup behind a double wire mesh partition in the homecage maintained aggression at a level identical to that of mothers in direct contact with their young. When placed behind the partition, unfamiliar 6, 13, and 20-day-old pups, but not 30-day-old mice, maintained the behavior as effectively as the dam's own young. The relationship of the findings to communal rearing conditions in the mouse is discussed.     

Nestling barn owls assess short-term variation in the amount of vocally competing siblings

Assessing the amount of rivals is crucial to optimally adjust investment into a contest. If laboratory animals show numerical abilities, little is known about the ecological implications particularly in young animals. The two to nine barn owl (Tyto alba) siblings vocally compete for priority of access to food resources before parents actually deliver them. In dyads, the individual that vocalizes at the highest rate in the absence of parents deters its siblings from competing for next delivered prey. We tested the novel hypothesis that to optimally adjust vocal investment, barn owl nestlings assess how many of their siblings are currently competing. To singleton owlets, we broadcasted a fixed global number of calls emitted by one, two or four pre-recorded unfamiliar nestlings. We could thus distinguish the independent effect on singletons’ vocal behavior of the global number of calls produced by a brood from the number of competitors that produced these calls. Overall, nestlings retreated more from vocal contest when facing more competitors. However, in front of one highly motivated competitor, nestlings refrained from vocalizing to a larger extent than when competing against more but less motivated individuals. Therefore, young animals assess variation in the number of currently competing siblings based on individual-specific vocal cues.     

Emerging effortful control in toddlerhood: the role of infant orienting/regulation, maternal effortful control, and maternal time spent in caregiving activities

Latent growth modeling (LGM) was used to examine the contribution of changes in infant orienting/regulation (O/R) to the emergence of toddler effortful control (EC), the contributions of maternal EC to the development of infant O/R and the emergence of toddler EC, the influence of maternal time spent in caregiving activities on toddler EC and the slope of infant O/R, and the contribution of maternal EC to subsequent maternal time spent in caregiving activities. Mothers from 158 families completed a self-report measure of EC when their infants were 4 months of age, a measure of infant O/R when their infants were 4, 6, 8, 10, and 12 months of age, and a measure of toddler EC when their children reached 18 months of age. Information concerning maternal time spent in various interactive caregiving activities was collected when infants were 6 months old. Results indicated higher maternal EC predicted interindividual differences in the intercept (i.e., higher intercepts), but not slope, of infant O/R and that higher maternal EC, higher infant O/R intercept, and higher infant O/R slope contributed to higher toddler EC. Furthermore, higher maternal EC predicted greater maternal time spent in interactive caregiving activities with their infants and greater maternal time in interactive caregiving with infants also contributed to higher toddler EC after controlling for maternal EC. These findings contribute to the understanding of the influence of maternal EC, directly and through caregiving, on toddler EC. Additional implications as they are related to early developing regulatory aspects of temperament are discussed.     

Emergence of an egocentric cue guiding and allocentric inferring strategy that mirrors hippocampal brain-derived neurotrophic factor (BDNF) expression in the Morris water maze

From insects to humans, successful navigation relies on retained representations of spatial relations. These representations are thought to depend on the hippocampal formation, particularly those that are independent of the navigator (allocentric representations). The Morris water maze is a simple and popular task often used to assess spatial navigation. But how animals navigate toward and retain information regarding the location of the goal in this task remains unclear. We provide a comprehensive account of how the water maze is accomplished behaviourally. Our findings suggest that animals solve the task using distal cues via an initial view-matching strategy that is supported by egocentric guidance. Through increased training, however, an emergence of an egocentric-guiding strategy combined with the animal’s greater ability to infer the hidden platform’s location (via allocentric extrapolation) emerges. We also demonstrate that behavioural changes, towards a more allocentric strategy, are reflected in increases in hippocampal brain-derived neurotrophic factor.     

You Get What You Need: An Examination of Purpose‐Based Inheritance Reasoning in Undergraduates,Preschoolers, and Biological Experts

This set of seven experiments examines reasoning about the inheritance and acquisition of physical properties in preschoolers, undergraduates, and biology experts. Participants (N = 390) received adoption vignettes in which a baby animal was born to one parent but raised by a biologically unrelated parent, and they judged whether the offspring would have the same property as the birth or rearing parent. For each vignette, the animal parents had contrasting values on a physical property dimension (e.g., the birth parent had a short tail; the rearing parent had a long tail). Depending on the condition, the distinct properties had distinct functions (“function‐predictive”) were associated with distinct habitats (“habitat‐predictive”), or had no implications (“non‐predictive”). Undergraduates' bias to view properties as inherited from the birth parent was reduced in the function‐ and habitat‐predictive conditions. This result indicates a purpose‐based view of inheritance, whereby animals can acquire properties that serve a purpose in their environment. This stance was not found in experts or preschoolers. We discuss the results in terms of how undergraduates' purpose‐based inheritance reasoning develops and relates to larger‐scale misconceptions about Darwinian evolutionary processes, and implications for biology education.     

Spatial navigation in complex and radial mazes in APP23 animals and neurotrophin signaling as a biological marker of early impairment

Impairment of hippocampal function precedes frontal and parietal cortex impairment in human Alzheimer's disease (AD). Neurotrophins are critical for behavioral performance and neuronal survival in AD. We used complex and radial mazes to assess spatial orientation and learning in wild-type and B6-Tg(ThylAPP)23Sdz (APP23) animals, a transgenic mouse model of AD. We also assessed brain content of nerve growth factor (NGF), brain-derived neurotrophic factor (BDNF), and neurotrophin-3 (NT-3). Performance was alike in wild-type and APP23 animals in the radial maze. In contrast, performance in the complex maze was better in wild-type than APP23 animals. Contrary to the wild-type, hippocampal BDNF levels decreased on training in APP23 animals. Hippocampal and frontal cortex NGF levels in APP23 animals correlated with the time to solve the complex maze, but correlated inversely with escape time in wild-type animals. NT-3 levels were alike in wild-type and APP23 animals and were unchanged even after training. Both types of mazes depend on hippocampal integrity to some extent. However, according to the cognitive mapping theory of spatial learning, the complex maze because of the increased complexity of the environment most likely depends more strongly on preserved hippocampal function than the radial maze in the working memory configuration applied here. Greater impairment in complex maze performance than in radial maze performance thus resembles the predominant affliction of the loss of hippocampal function in human AD. NGF and BDNF levels on maze learning are different in wild-type and transgenic animals, indicating that biological markers of AD may be altered on challenge even though equilibrium levels are alike.     

Fragile X mental retardation protein levels increase following complex environment exposure in rat brain regions undergoing active synaptogenesis

Fragile X mental retardation protein (FMRP), which is absent in fragile X syndrome, is synthesized in vitro in response to neurotransmitter activation. Humans and mice lacking FMRP exhibit abnormal dendritic spine development, suggesting that this protein plays an important role in synaptic plasticity. Previously, our laboratory demonstrated increased FMRP immunoreactivity in visual cortex of rats exposed to complex environments (EC) and in motor cortex of rats trained on motor-skill tasks compared with animals reared individually in standard laboratory housing (IC). Here, we use immunohistochemistry to extend those findings by investigating FMRP levels in visual cortex and hippocampal dentate gyrus of animals exposed to EC or IC. Rats exposed to EC for 20 days exhibited increased FMRP immunoreactivity in visual cortex compared with animals housed in standard laboratory caging. In the dentate gyrus, animals exposed to EC for 20 days had higher FMRP levels than animals exposed to EC for 5 or 10 days. In light of possible antibody crossreactivity with closely related proteins FXR1P and FXR2P, FMRP immunoreactivity in the posterior-dorsal one-third of cerebral cortex was also examined by Western blotting following 20 days of EC exposure. FMRP levels were greater in EC animals, whereas levels of FXR1P and FXR2P were unaffected by experience. These results provide further evidence for behaviorally induced alteration of FMRP expression in contrast to its homologues, extend previous findings suggesting regulation of its expression by synaptic activity, and support the theories associating FMRP expression with alteration of synaptic structure both in development and later in the life-cycle.     

Effects of NGF, b-FGF, and cerebrolysin on water maze performance and on motor activity of rats: short- and long-term study

The effects of 14-day treatments with nerve growth factor (NGF), basic fibroblast growth factor (b-FGF), or the peptidergic drug Cerebrolysin on postlesion acquisition of a water maze task and on motor activity were evaluated. Rats were tested in the Morris water maze 14 days (early test) and 7 to 8 months (delayed test) after a bilateral lesion of the frontoparietal (sensorimotor) cortex. Only the rats treated with Cerebrolysin performed the water maze task at the level of the nonlesioned controls in the early test. No short-term effect of NGF (6.5 ng/14 days; 38 ng/ml) or b-FGF (17 ng/14 days; 100 ng/ml) treatment was found. The delayed test revealed that water maze performance was restored in rats treated with b-FGF in comparison with intact controls. The data showed that b-FGF can support or initiate processes in the CNS that lead to a delayed functional amelioration and/or compensation for a water maze performance deficit. NGF did not influence the acquisition impairment caused by a sensorimotor cortical lesion. Two-week administration of Cerebrolysin had a time-dependent influence: it attenuated the acquisition deficit and increased the motor activity of rats, both effects declined to the level of lesioned controls within 8 months.