Reward type influences performance and search structure of an omnivorous bird in an open-field maze

Open-field mazes are routinely used to study the spatial cognitive abilities of birds and are often implicitly assumed to be suitable tests of generic spatial memory ability. In recent years there has been extensive research motivated by considerations of an animals’ ecology, demonstrating potential examples of specialisations of spatial cognition, as a result of foraging niche. The study reported here demonstrates differences in maze performance as a function of reward type (nectar and invertebrates) that can be predicted from the natural distributions of these rewards. As well as specific implications for the nature of spatial memory specialisation in this species, the results hold more general implications for the use of open-field mazes as tools for measuring and comparing spatial memory ability between species.     

Some characteristics of spatial associative memory in the pigeon, Columba livia

Willson and Wilkie (1993) developed a novel procedure to assess pigeons' memory for the spatial location of food. Only one of four locations provided food each daily session. Each location consisted of an illuminated pecking key and grain feeder. Over different days different locations, randomly selected, provided food during a 16-min session. The pigeons tended to revisit the location at which food was found on the previous day thereby demonstrating memory for food-spatial location associations over 24 h. Three experiments were conducted to further investigate this phenomenon. In Experiment 1 the session duration was varied between 4 and 32 min. Longer sessions had no detectable effect on their ability to remember the rewarded location 24 h later, a result that suggests that only brief encounters with food at a particular location are necessary for recall. In Experiment 2 the necessity of an active search for the day's rewarded location was removed; a 5-min period in which only the rewarded key was lit preceded the regular 16-min session. Pecks to the lit key in this 5-min period produced grain on the standard schedule. This manipulation facilitated the pigeons' discovery of food but did not affect their ability to remember the rewarded location, suggesting that the process of search and discovery is not essential to the associative memory process. In Experiment 3, food was available during the complete session (non-depleting condition) or was available only during the first half of the session (depleting condition). No detectable differences in the birds' memory of yesterday's profitable location were found. This suggests that non-depletion of food is not a necessary condition for day-to-day recall of food location. Taken together these findings enlarge our understanding of the spatial associative memory process.     

Vasopressin analogues and spatial working memory in the 24-arm radial maze

The effect of vasopressin analogues dAVP, dDAVP, and desgly NH₂ dDAVP on working memory was tested in the 24-arm radial maze in twelve 6-month-old and twelve 19-month-old rats. No age dependent effects were found. All three peptides tested (3 μg/kg) tended to improve the performance but only the desgly NH₂ dDAVP significantly decreased the number of errors. A second application of desgly NH₂ dDAVP was ineffective. The specificity of activation of memory mechanisms by desgly NH₂ dDAVP can be questioned.     

An assessment of Gallistel's (2012) rationalistic account of extinction phenomena

Gallistel (2012) asserts that animals use rationalistic reasoning (i.e., information theory and Bayesian inference) to make decisions that underlie select extinction phenomena. Rational processes are presumed to lead to evolutionarily optimal behavior. Thus, Gallistel's model is a type of optimality theory. But optimality theory is only a theory, a theory about an ideal organism, and its predictions frequently deviate appreciably from observed behavior of animals in the laboratory and the real world. That is, behavior of animals is often far from optimal, as is evident in many behavioral phenomena. Hence, appeals to optimality theory to explain, rather than illuminate, actual behavior are misguided.     

Inhibiting DNA methylation alters olfactory extinction but not acquisition learning in Apis cerana and Apis mellifera

DNA methylation plays a key role in invertebrate acquisition and extinction memory. Honey bees have excellent olfactory learning, but the role of DNA methylation in memory formation has, to date, only been studied in Apis mellifera. We inhibited DNA methylation by inhibiting DNA methyltransferase (DNMT) with zebularine (zeb) and studied the resulting effects upon olfactory acquisition and extinction memory in two honey bee species, Apis cerana and A. mellifera. We used the proboscis extension reflex (PER) assay to measure memory. We provide the first demonstration that DNA methylation is also important in the olfactory extinction learning of A. cerana. DNMT did not reduce acquisition learning in either species. However, zeb bidirectionally and differentially altered extinction learning in both species. In particular, zeb provided 1 h before acquisition learning improved extinction memory retention in A. mellifera, but reduced extinction memory retention in A. cerana. The reasons for these differences are unclear, but provide a basis for future studies to explore species-specific differences in the effects of methylation on memory formation.     

Microwave irradiation affects radial-arm maze performance in the rat

After 45 min of exposure to pulsed 2450 MHz microwaves (2 μsec pulses, 500 pps, 1 mW/cm², average whole body SAR 0.6 W/kg), rats showed retarded learning while performing in the radial-arm maze to obtain food rewards, indicating a deficit in spatial “working memory” function. This behavioral deficit was reversed by pretreatment before exposure with the cholinergic agonist physostigmine or the opiate antagonist naltrexone, whereas pretreatment with the peripheral opiate antagonist naloxone methiodide showed no reversal of effect. These data indicate that both cholinergic and endogenous opioid neurotransmitter systems in the brain are involved in the microwave-induced spatial memory deficit. © 1994 Wiley-Liss, Inc.     

Eliminating the adrenal stress response does not affect sleep deprivation-induced acquisition deficits in the water maze

Sleep deprivation impairs spatial learning in the rat. Sleep deprivation, however, also causes stress and stress itself can interfere with spatial learning. To address this confound, sleep deprivation effects on Morris water maze training were studied in intact rats and in rats in which the adrenal stress response had been eliminated by adrenalectomy. Stable, physiological levels of corticosterone were maintained in adrenalectomized rats with an implanted pellet. Training occurred 6-7 days after surgery. Seventy-two hours sleep deprivation by the platform-over-water method just prior to training slowed, but did not block, learning. In particular, the robust savings between trials 1 and 2 of the first set found in home cage rats was not present in sleep-deprived rats. Adrenalectomy/corticosterone replacement surgery did not modify the effect of sleep deprivation on acquisition rate, demonstrating that the deficits in spatial task acquisition due to pre-training sleep deprivation are not secondary to the adrenal stress response.     

Evidence for the influence of testosterone in the performance of spatial navigation in a virtual water maze in women but not in men

Testosterone (T) may be associated with enhanced spatial navigation in a number of rodent species, although the nature of the relation is equivocal. Similarly, numerous studies in humans generally have found that T is associated with enhanced spatial ability on a variety of paper and pencil tasks that may relate to navigational ability. However, relatively few studies have reported effects of T on navigational ability in humans. We investigated the relationship between endogenous T and performance on a virtual water maze (vWM) and mental rotations test (MROT). ELISA for T was performed on salivary samples that were obtained from participants before and after completion of both spatial tasks. Results indicated that women with low T required more time to locate the hidden platform in the vWM than either group of men or women with high T. Significant negative correlations were found for the entire sample between vWM performance and T, and between vWM latency to escape and MROT. Similar significant correlations were found in women but not men. Thus, our data support the position that T improves performance in the vWM in a linear fashion, most strongly in women. However, further work is needed to confirm this hypothesis in humans.     

Effects of testosterone on spatial learning and memory in adult male rats

A male advantage over females for spatial tasks has been well documented in both humans and rodents, but it remains unclear how the activational effects of testosterone influence spatial ability in males. In a series of experiments, we tested how injections of testosterone influenced the spatial working and reference memory of castrated male rats. In the eight-arm radial maze, testosterone injections (0.500 mg/rat) reduced the number of working memory errors during the early blocks of testing but had no effect on the number of reference memory errors relative to the castrated control group. In a reference memory version of the Morris water maze, injections of a wide range of testosterone doses (0.0625-1.000 mg/rat) reduced path lengths to the hidden platform, indicative of improved spatial learning. This improved learning was independent of testosterone dose, with all treatment groups showing better performance than the castrated control males. Furthermore, this effect was only observed when rats were given testosterone injections starting 7 days prior to water maze testing and not when injections were given only on the testing days. We also observed that certain doses of testosterone (0.250 and 1.000 mg/rat) increased perseverative behavior in a reversal-learning task. Finally, testosterone did not have a clear effect on spatial working memory in the Morris water maze, although intermediate doses seemed to optimize performance. Overall, the results indicate that testosterone can have positive activational effects on spatial learning and memory, but the duration of testosterone replacement and the nature of the spatial task modify these effects.     

Effect of intrahippocampal administration of anti-melanin-concentrating hormone on spatial food-seeking behavior in rats

Melanin-concentrating hormone (MCH) is a hypothalamic peptide that plays a critical role in the regulation of food intake and energy metabolism. In this study, we investigated the potential role of dense hippocampal MCH innervation in the spatially oriented food-seeking component of feeding behavior. Rats were trained for eight sessions to seek food buried in an arena using the working memory version of the food-seeking behavior (FSB) task. The testing day involved a bilateral anti-MCH injection into the hippocampal formation followed by two trials. The anti-MCH injection did not interfere with the performance during the first trial on the testing day, which was similar to the training trials. However, during the second testing trial, when no food was presented in the arena, the control subjects exhibited a dramatic increase in the latency to initiate digging. Treatment with an anti-MCH antibody did not interfere with either the food-seeking behavior or the spatial orientation of the subjects, but the increase in the latency to start digging observed in the control subjects was prevented. These results are discussed in terms of a potential MCH-mediated hippocampal role in the integration of the sensory information necessary for decision-making in the pre-ingestive component of feeding behavior.     

Effects of genistein in the maternal diet on reproductive development and spatial learning in male rats

Endocrine disruptors, chemicals that disturb the actions of endogenous hormones, have been implicated in birth defects associated with hormone-dependent development. Phytoestrogens are a class of endocrine disruptors found in plants. In the current study we examined the effects of exposure at various perinatal time periods to genistein, a soy phytoestrogen, on reproductive development and learning in male rats. Dams were fed genistein-containing (5 mg/kg feed) food during both gestation and lactation, during gestation only, during lactation only, or during neither period. Measures of reproductive development and body mass were taken in the male offspring during postnatal development, and learning and memory performance was assessed in adulthood. Genistein exposure via the maternal diet decreased body mass in the male offspring of dams fed genistein during both gestation and lactation, during lactation only, but not during gestation only. Genistein decreased anogenital distance when exposure was during both gestation and lactation, but there was no effect when exposure was limited to one of these time periods. Similarly, spatial learning in the Morris water maze was impaired in male rats exposed to genistein during both gestation and lactation, but not in rats exposed during only one of these time periods. There was no effect of genistein on cued or contextual fear conditioning. In summary, the data indicate that exposure to genistein through the maternal diet significantly impacts growth in male offspring if exposure is during lactation. The effects of genistein on reproductive development and spatial learning required exposure throughout the pre- and postnatal periods.     

Developmental exposure to xenoestrogen enhances spatial learning in male rats

Steroid hormones have profound effects on the development and function of the nervous system. Environmental estrogens or xenoestrogens are manmade or are natural compounds, which mimics the action of estrogen hormones. The experimental evidence for impairment of cognitive functions in humans and mammals following exposure to xenoestrogens has been fiercely debated. The strongest arguments against such studies have been that the route, time course, and intensity of exposure did not simulate environmental exposure, and that the chemicals tested have additional, non-estrogenic toxic effects, hindering a generalization of actual "xenoestrogenic" effects. Here we show that an environmental-like exposure to the pure estrogen, 17alpha-ethynylestradiol (EE2) during development enhances spatial learning abilities in adult male Sprague-Dawley rats. To simulate an environmental exposure, we used a very low dose (4 ng/kg/day) of EE2 equivalent to concentrations measured in European and US streams which was given orally with a non-invasive method, and we extended the treatment for the entire course of development, from conception to puberty. The animals were tested in a Morris water maze protocol at 6 months of age. Male rats treated with EE2 during development showed a faster learning during the training phase, and remembered better the position of the hidden platform in the short term. Our study demonstrates that actual levels of exposure to xenoestrogens can permanently alter cognitive abilities of a mammalian species.     

Effects of pregnancy on spatial cognition in female Hooded Long-Evans rats

Studies examining the roles of estrogens and progestins on spatial cognition have been highly contradictory. To determine if the hormonal environment of pregnancy affects spatial cognition, pregnant (n = 7) and virgin (n = 7) Hooded Long-Evans rats were tested in a Morris water maze throughout the 3 weeks of pregnancy and the second week postpartum. Latency to platform, path length, swim velocity, and time in quadrant were compared over trial-days. To compare water maze performance with changes in hormone levels, serum concentrations of estradiol and progesterone were measured on the first, third, and fifth days of testing during the third week of pregnancy. Subjects learned to find the platform as indicated by decreased time and distance to platform over each trial-week and increased time spent in the quadrant where the platform had been located the previous week. However, there were no differences between treatment groups on time or distance to platform over trial-days. Swim velocity did not differ between or within groups over the 4 weeks of testing. Although primigravid and virgin females were similar in their abilities to learn the novel location of a submerged platform and return to it over time, pregnant animals demonstrated less perseveration to previously learned information and were quicker to locate the platform when it moved to a new location. Thus, reproductive status did not affect reference memory but enhanced working memory in the Morris water maze.     

Assessment of estradiol influence on spatial tasks and hippocampal CA1 spines: evidence that the duration of hormone deprivation after ovariectomy compromises 17beta-estradiol effectiveness in altering CA1 spines

Two pulses of 17β-estradiol (10 µg) are commonly used to increase hippocampal CA1 apical dendritic spine density and alter spatial performance in ovariectomized (OVX) female rats, but rarely are the measures combined. The goal of this study was to use this two-pulse injection protocol repeatedly with intervening wash-out periods in the same rats to: 1) measure spatial ability using different tasks that require hippocampal function and 2) determine whether ovarian hormone depletion for an extended 10-week period reduces 17β-estradiol's effectiveness in elevating CA1 apical dendritic spine density. Results showed that two injections of 10 µg 17β-estradiol (72 and 48 h prior to testing and timed to maximize CA1 apical spine density at behavioral assessment) corresponded to improved spatial memory performance on object placement. In contrast, two injections of 5 µg 17β-estradiol facilitated spatial learning on the water maze compared to rats given two injections of 10 µg 17β-estradiol or the sesame oil vehicle. Neither 17β-estradiol dose altered Y-maze performance. As expected, the intermittent two-pulse injection protocol increased CA1 apical spine density, but 10 weeks of OVX without estradiol treatment decreased the effectiveness of 10 µg 17β-estradiol to increase CA1 apical spine density. Moreover, two pulses of 5 µg 17β-estradiol injected intermittently failed to alter CA1 apical spine density and decreased basal spine density. These results demonstrate that extended time without ovarian hormones reduces 17β-estradiol's effectiveness to increase CA1 apical spine density. Collectively, these findings highlight the complex interactions among estradiol, CA1 spine density/morphology, and task requirements, all of which contribute to behavioral outcomes.     

Roles of oxytocin in spatial learning and memory in the nucleus basalis of Meynert in rats

The present study was performed to explore the role of oxytocin (OT) in spatial learning and memory in the nucleus basalis of Meynert (NBM) of rats. The latency, distance and swimming path to find the platform were tested by Morris water maze and recorded by a video camera connected to a computer. Intra-NBM injections of 2 or 10 nmol of OT, but not 0.2 nmol of OT, induced significant increase on the latency of spatial learning. Rats receiving intra-NBM administrations of 2 or 10 nmol of OT showed a more random search pattern. There were no significant changes in the swimming speed in Morris water maze test after the injection of OT. Furthermore, the impaired effect of OT on the latency of spatial learning was blocked by intra-NBM injection of the selective OT antagonist Atosiban, indicating that the effect of OT was mediated by OT receptor in the NBM of rats. Moreover, there were no influences of OT or Atosiban on the retention performance in rats. The results suggest that OT plays an inhibitory role in spatial learning in the NBM; the effect is mediated by OT receptor.     

Blocking of spatial control by landmarks in rats

We investigated spatial blocking among landmarks in an open-field foraging task in rats. In Phase 1, rats were presented with A+ trials during which landmark (LM) A signaled the location of hidden food. In Phase 2, rats were given AX+ trials in which LM X served as a redundant spatial cue to the location of food. Additionally, BY+ trials were given as a within-subjects overshadowing-control procedure. At test, rats received nonreinforced presentations of LM X and LM Y on separate trials. Rats took longer to find the training goal location in the presence of LM X than of LM Y, thereby demonstrating that spatial control by LM X was blocked by prior learning with LM A. This constitutes the first evidence in rats for spatial blocking of one proximal landmark by another—approximating a conventional blocking design.     

Changes in vascular endothelial growth factor (VEGF) induced by the Morris water maze task

The present study was undertaken to evaluate the effects on hippocampal vascular endothelial growth factor (VEGF) levels in rats when they experience hippocampal-dependent spatial learning via the Morris water maze (MWM) task. Rats underwent one of two different versions of the MWM: weak or intensive. After one day of intensive training, a highly sensitive enzyme-linked immunosorbent assay (ELISA) was used to measure VEGF protein levels in the hippocampus, cortex, and serum, and higher levels were found in the trained group compared to a naive control group. VEGF levels also increased in rats that swam only for durations equal to the intensive training periods. In contrast, rats trained under the weaker MWM paradigm for five days showed a decrease in hippocampal VEGF protein level. Mimicking increases in neuronal VEGF in the hippocampus by direct infusion of VEGF into CA1 resulted in up-regulation of the phosphorylation of the cAMP response element-binding (CREB) protein and the Ca²⁺/calmodulin-dependent protein kinases II (CaMKII). These results suggest that VEGF may be a physiological parameter involved in learning procedures that include physical activity.     

Associative learning in biochemical networks

It has been recently suggested that there are likely generic features characterizing the emergence of systems constructed from the self-organization of self-replicating agents acting under one or more selection pressures. Therefore, structures and behaviors at one length scale may be used to infer analogous structures and behaviors at other length scales. Motivated by this suggestion, we seek to characterize various "animate" behaviors in biochemical networks, and the influence that these behaviors have on genomic evolution. Specifically, in this paper, we develop a simple, chemostat-based model illustrating how a process analogous to associative learning can occur in a biochemical network. Associative learning is a form of learning whereby a system "learns" to associate two stimuli with one another. Associative learning, also known as conditioning, is believed to be a powerful learning process at work in the brain (associative learning is essentially "learning by analogy"). In our model, two types of replicating molecules, denoted as A and B, are present in some initial concentration in the chemostat. Molecules A and B are stimulated to replicate by some growth factors, denoted as G(A) and G(B), respectively. It is also assumed that A and B can covalently link, and that the conjugated molecule can be stimulated by either the G(A) or G(B) growth factors (and can be degraded). We show that, if the chemostat is stimulated by both growth factors for a certain time, followed by a time gap during which the chemostat is not stimulated at all, and if the chemostat is then stimulated again by only one of the growth factors, then there will be a transient increase in the number of molecules activated by the other growth factor. Therefore, the chemostat bears the imprint of earlier, simultaneous stimulation with both growth factors, which is indicative of associative learning. It is interesting to note that the dynamics of our model is consistent with certain aspects of Pavlov's original series of conditioning experiments in dogs. We discuss how associative learning can potentially be performed in vitro within RNA, DNA, or peptide networks. We also describe how such a mechanism could be involved in genomic evolution, and suggest relevant bioinformatics studies that could potentially resolve these issues.     

Repeated extinction and reversal learning of an approach response supports an arousal-mediated learning model

We assessed the effects of repeated extinction and reversals of two conditional stimuli (CS+/CS−) on an appetitive conditioned approach response in rats. Three results were observed that could not be accounted for by a simple linear operator model such as the one proposed by Rescorla and Wagner (1972): (1) responding to a CS− declined faster when a CS+ was simultaneously extinguished; (2) reacquisition of pre-extinction performance recovered rapidly within one session; and (3) reversal of CS+/CS− contingencies resulted in a more rapid recovery to the current CS− (former CS+) than the current CS+, accompanied by a slower acquisition of performance to the current CS+. An arousal parameter that mediates learning was introduced to a linear operator model to account for these effects. The arousal-mediated learning model adequately fit the data and predicted data from a second experiment with different rats in which only repeated reversals of CS+/CS− were assessed. According to this arousal-mediated learning model, learning is accelerated by US-elicited arousal and it slows down in the absence of US. Because arousal varies faster than conditioning, the model accounts for the decline in responding during extinction mainly through a reduction in arousal, not a change in learning. By preserving learning during extinction, the model is able to account for relapse effects like rapid reacquisition, renewal, and reinstatement.     

Stochastic growth and extinction in a spatial geometric Brownian population model with migration and correlated noise

A continuous spatial model for populations that are not density-regulated is analyzed. The model is a generalization of the geometric Brownian motion often used to describe populations at a single location. The locations are linked by migration and spatial correlation in the noise. At any point of time, the population size at a given location is log normally distributed so the log population size constitutes a Gaussian field. The model is homogeneous in space but not in time. In particular, we analyze the case when the stochastic growth rate is negative and the total population approaches extinction. The properties of the extinction process is studied by considering local quasi-extinctions. A major conclusion is that migration tends to increase the time to extinction provided that there is no cost of migration. However, as the area occupied by the species starts to decrease, the decrease is faster for populations with larger migration.