Lateralization and unilateral transfer of spatial memory in marsh tits: are two eyes better than one?

Two previous experiments on food storing and one-trial associative learning in marsh tits (Clayton 1992a; Clayton and Krebs 1992) demonstrate that information coming into the brain from the left eye disappears from the left eye system between 3 and 24 h after memory formation, whereas that coming into the brain from the right eye remains stable within the right eye system for at least 51 h after memory formation. Performance after a 7 h retention interval appears to represent an intermediate stage in which the information is no longer accessible to the left eye system but is not yet available to the right eye system, suggesting a unilateral transfer of memory. The experiments reported here further investigated lateralization and unilateral transfer of memory in food-storing marsh tits, Parus palustris, using the technique of monocular occlusion. Birds were tested for their ability to retrieve stored seeds after retention intervals of 3, 7 and 24 h under 4 different occlusion treatments. Two predictions were tested: (a) with right eye occlusion during storage, birds should show better memory performance after 3 and 24 h than after 7 h and (b) memory should be more accurate when both eyes are used during storage than with monocular occlusion. The first prediction, which arises from the fact that memory is transferred from the left to the right eye system at about 7 h and is inaccessible during the transfer, was supported by the data. The second prediction, however, was not supported. Previous work has shown that in marsh tits the two eye systems remember preferentially different aspects of the stimulus: the left eye system responds to spatial position and the right eye system to object-specific cues. It is possible that the failure to find superior performance in binocular tests was because the task could be solved by either spatial or object-specific memory.     

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.     

Memory for the location of stored food in marsh tits

Marsh tits store several hundred food items per day, in separate locations within their territory, and recover most items within 24 h. Experiments in the laboratory determined that marsh tits return accurately to the sites of stored sunflower seeds 3 h and 24 h after storage. The proportion of returns exceeded chance encounter and initial preferences for those sites. The lack of interocular transfer in birds for some visual tasks provided a test for the hypothesis that memory is used to relocate stored food. After storing food with one eye covered, marsh tits did not return to storage sites when using only the ‘naive’ eye, but did so when using only the eye uncovered during storage. It seems likely that recovery of stored food by marsh tits and other birds occurs by memory of storage sites, not by chance encounter during foraging.     

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.     

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.     

The relationship between migratory behaviour, memory and the hippocampus: an intraspecific comparison

It has been hypothesized that memory-demanding ecological conditions might result in enhanced memory and an enlarged hippocampus, an area of the brain involved in memory processing, either via extensive memory experience or through evolutionary changes. Avian migration appears to represent one of such memory-demanding ecological conditions. We compared two subspecies of the white-crowned sparrow: migratory Zonotrichia leucophrys gambelii and non-migratory Z. l. nuttalli. Compared to non-migratory Z. l. nuttalli, migratory Z. l. gambelii showed better memory performance on spatial one-trial associative learning tasks and had more hippocampal neurons. Migratory subspecies also had larger hippocampi relative to the remainder of the telencephalon but not relative to body mass. In adults, the differences between migratory and non-migratory sparrows were especially pronounced in the right hippocampus. Juvenile migratory Z. l. gambelii had relatively larger hippocampal volume compared to juvenile non-migratory Z. l. nuttalli. Adult migratory Z. l. gambelii had more neurons in their right hippocampus compared to juveniles but such differences were not found in non-migratory Z. l. nuttalli. Our results suggest that migratory behaviour might be related to enhanced spatial memory and an enlarged hippocampus with more neurons, and that differences in the hippocampus between migratory and non-migratory sparrows might be experience-dependent. Furthermore, for the first time our results suggest that the right hippocampus, which encodes global spatial information, might be involved in migratory behaviour.     

Effects of demanding foraging conditions on cache retrival accuracy in food-caching mountain chickadees (Poecile gambeli)

Birds rely, at least in part, on spatial memory for recovering previously hidden caches but accurate cache recovery may be more critical for birds that forage in harsh conditions where the food supply is limited and unpredictable. Failure to find caches in these conditions may potentially result in death from starvation. In order to test this hypothesis we compared the cache recovery behaviour of 24 wild-caught mountain chickadees (Poecile gambeli), half of which were maintained on a limited and unpredictable food supply while the rest were maintained on an ad libitum food supply for 60 days. We then tested their cache retrieval accuracy by allowing birds from both groups to cache seeds in the experimental room and recover them 5 hours later. Our results showed that birds maintained on a limited and unpredictable food supply made significantly fewer visits to non-cache sites when recovering their caches compared to birds maintained on ad libitum food. We found the same difference in performance in two versions of a one-trial associative learning task in which the birds had to rely on memory to find previously encountered hidden food. In a non-spatial memory version of the task, in which the baited feeder was clearly marked, there were no significant differences between the two groups. We therefore concluded that the two groups differed in their efficiency at cache retrieval. We suggest that this difference is more likely to be attributable to a difference in memory (encoding or recall) than to a difference in their motivation to search for hidden food, although the possibility of some motivational differences still exists. Overall, our results suggest that demanding foraging conditions favour more accurate cache retrieval in food-caching birds.     

Rat spatial memory tasks adapted for humans: characterization in subjects with intact brain and subjects with selective medial temporal lobe thermal lesions

In the present paper we describe five tests, 3 of which were designed to be similar to tasks used with rodents. Results obtained from control subjects, patients with selective thermo-coagulation lesions to the medial temporal lobe and results from non-human primates and rodents are discussed. The tests involve memory for spatial locations acquired by moving around in a room, memory for objects subjects interacted with, or memory for objects and their locations. Two of the spatial memory tasks were designed specifically as analogs of the Morris water task and the 8-arm radial-maze tasks used with rats. The Morris water task was modeled by hiding a sensor under the carpet of a room (Invisible Sensor Task). Subjects had to learn its location by using an array of visual cues available in the room. A path integration task was developed in order to study the non-visual acquisition of a cognitive representation of the spatial location of objects. In the non-visual spatial memory task, we blindfolded subjects and led them to a room where they had to find 3 objects and remember their locations. We designed an object location task by placing 4 objects in a room that subjects observed for later recall of their locations. A recognition task, and a novelty detection task were given subsequent to the recall task. An 8-arm radial-maze was recreated by placing stands at equal distance from each other around the room, and asking subjects to visit each stand once, from a central point. A non-spatial working memory task was designed to be the non-spatial equivalent of the radial maze. Search paths recorded on the first trial of the Invisible Sensor Task, when subjects search for the target by trial and error are reported. An analysis of the search paths revealed that patients with lesions to the right or left hippocampus or parahippocampal cortex employed the same type of search strategies as normal controls did, showing similarities and differences to the search behavior recorded in rats. Interestingly, patients with lesions that included the right parahippocampal cortex were impaired relative to patients with lesions to the right hippocampus that spared the parahippocampal cortex, when recall of the sensor was tested after a 30 min delay (Bohbot et al. 1998). No differences were obtained between control subjects and patients with selective thermal lesions to the medial temporal lobe, when tested on the radial-maze, the non-spatial analogue to the radial-maze and the path integration tasks. Differences in methodological procedures, learning strategies and lesion location could account for some of the discrepant results between humans and non-human species. Patients with lesions to the right hippocampus, irrespective of whether the right parahippocampal cortex was spared or damaged, had difficulties remembering the particular configuration and identity of objects in the novelty detection of the object location task. This supports the role of the human right hippocampus for spatial memory, in this case, involving memory for the location of elements in the room; learning known to require the hippocampus in the rat.     

Food storage by black-capped chickadees: Memory for the location and contents of caches

Black-capped chickadees (Parus atricapillus) store food in a scattered distribution in their winter home range. Several hundred food items may be stored in a day, each in a separate cache site. Previous studies of marsh tits (Parus palustris) and nutcrackers (Nucifraga spp.) have shown that spatial memory is used to relocate caches. Memory for storage sites, if used by black-capped chickadees, is predicted to have four properties. Birds should be able to: (1) accurately relocate cache sites, (2) recall which caches they have previously emptied, (3) recall which sites they have discovered empty (as a result of loss to other animals) and (4) recall what type of food is stored at a cache site. Laboratory experiments show that chickadees do incorporate these kinds of information in memory for cache sites.     

Persistence of long-term memory storage requires a late protein synthesis- and BDNF- dependent phase in the hippocampus

Persistence is the most characteristic attribute of long-term memory (LTM). To understand LTM, we must understand how memory traces persist over time despite the short-lived nature and rapid turnover of their molecular substrates. It is widely accepted that LTM formation is dependent upon hippocampal de novo protein synthesis and Brain-Derived Neurotrophic Factor (BDNF) signaling during or early after acquisition. Here we show that 12 hr after acquisition of a one-trial associative learning task, there is a novel protein synthesis and BDNF-dependent phase in the rat hippocampus that is critical for the persistence of LTM storage. Our findings indicate that a delayed stabilization phase is specifically required for maintenance, but not formation, of the memory trace. We propose that memory formation and memory persistence share some of the same molecular mechanisms and that recurrent rounds of consolidation-like events take place in the hippocampus for maintenance of the memory trace.     

Reverse lateralization of visual discriminative abilities in the European starling

Previous experiments on visual feature discrimination abilities have consistently shown a right-eye system lateralization in pigeons, Columba livia, and young domestic chickens, Gallus gallus domesticus, both nonpasserine species. Recently, however, it has been shown that photoreceptor distribution in the left and right retinas are asymmetrical in the European starling, Sturnus vulgaris, a passerine species. Single cone receptors are significantly more abundant in the left retina, which suggests that starlings should perform visual discrimination tasks more proficiently with the left eye, in contrast to previous findings with nonpasserines. We tested this hypothesis using the technique of monocular occlusion. In the first experiment, starlings were tested on a simultaneous visual discrimination task in three conditions: binocular (both eyes), left monocular (left eye only) and right monocular (right eye only). Subjects in the binocular and left-monocular conditions achieved significantly higher performance scores on the discrimination task than birds in the right-monocular condition. A second experiment found similar results, with birds in the left-monocular condition learning the discrimination task more than twice as quickly as those in the right-monocular condition. Subsequent tests with the alternative eye for both groups indicated no interocular transfer. These findings suggest that visual discriminative abilities in starlings are asymmetrical, and that they are lateralized in the opposite eye system than has been reported for all other species tested to date.     

Stereotypic route-tracing in experimentally caged songbirds correlates with general behavioural disinhibition

Repetitive, unvarying and apparently functionless behaviours called stereotypies are common in caged animals, but the mechanisms of cage stereotypy have remained elusive. We found that stereotypies correlate with a sign of altered brain functioning, the general disinhibition of behaviour, found in stereotyping human patients and animals treated with psychostimulants. We investigated route-tracing stereotypy in blue tits, Parus caeruleus, and marsh tits,P. palustris , caged in a behavioural research laboratory. In experiment 1, stereotypy correlated with disinhibition of responses, shown as persistent responding in extinction learning. In experiment 2a, stereotypy in blue tits correlated with repetitive sequence generation on a ‘gambling task’ that specifically measures disinhibited striatal functioning in humans and correlates with stereotypy in autistic and schizophrenic patients. In experiment 2b, the behavioural disinhibition correlated with stereotypy also affected food-storing behaviour in marsh tits, in particular their response to cache pilfering. In experiment 3, the sequencing of nonstereotypic home cage behaviour was correlated with stereotypy. Finally, changes in stereotypy induced by environmental enrichment correlated with changes in these measures of altered behavioural control. These results suggest that housing conditions that cause stereotypy thus alter many aspects of the behavioural control of caged subjects, mediated by altered striatal functioning. The implications for understanding cage stereotypies in laboratory, farm and zoo animals, and for laboratory-based behavioural experiments, are discussed. We suggest that improving housing conditions so that cage stereotypies do not develop would enhance the validity of laboratory-based behavioural research.     

Super-Memorizers Are Not Super-Recognizers

Humans have a natural expertise in recognizing faces. However, the nature of the interaction between this critical visual biological skill and memory is yet unclear. Here, we had the unique opportunity to test two individuals who have had exceptional success in the World Memory Championships, including several world records in face-name association memory. We designed a range of face processing tasks to determine whether superior/expert face memory skills are associated with distinctive perceptual strategies for processing faces. Superior memorizers excelled at tasks involving associative face-name learning. Nevertheless, they were as impaired as controls in tasks probing the efficiency of the face system: face inversion and the other-race effect. Super memorizers did not show increased hippocampal volumes, and exhibited optimal generic eye movement strategies when they performed complex multi-item face-name associations. Our data show that the visual computations of the face system are not malleable and are robust to acquired expertise involving extensive training of associative memory.     

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.     

Lateralization When Monitoring Predators in the Wild: A Left Eye Control in the Common Wall Lizard (Podarcis muralis)

Lateralization is the function specialization between left and right brain hemispheres. It is now ascertained in ectotherms too, where bias in eye use for different tasks, i.e., visual lateralization, is widespread. The lateral eye position on the head of ectotherm animals, in fact, allows them to observe left/right stimuli independently and allows lateralized individuals to carry out left and right perceived tasks at the same time. A recent study conducted on common wall lizards, Podarcis muralis, showed that lizards predominantly monitor a predator with the left eye while escaping. However, this work was conducted in a controlled laboratory setting owing to the difficulty of carrying out lateralization experiments under natural conditions. Nevertheless, field studies could provide important information to support what was previously found in the laboratory and demonstrate that these traits occur in nature. In this study, we conducted a field study on the antipredatory behavior of P. muralis lizards. We simulated predatory attacks on lizards in their natural environment. We found no lateralization in the measure of eye used by the lizard to monitor the predator before escaping from it, but the eye used was probably determined by the relative position of the lizard and the predator just before the attack. This first eye used did not affect escape decisions; lizards chose to escape toward the nearest refuge irrespective of whether it was located to the lizard’s left or right side. However, once they had escaped to a refuge, lizards had a left eye–mediated bias to monitor the predator when first emerging from the refuge, and this bias was likely independent of other environmental variables. Hence, these field findings support a left eye–mediated observation of the predator in P. muralis lizards, which confirms previous findings in this and other species.     

Effects of Lanthanum Chloride Administration in Prenatal Stage on One-Trial Passive Avoidance Learning in Chicks

Lanthanum cations (La 3+) are well known for their inhibitory actions on calcium channels. Prenatal lanthanum exposure may affect the development of embryo and alter the capacity for learning and memory in adults, and the one-trial passive avoidance learning paradigm with day-old chicks is an excellent model to study several mechanisms of memory formation. In the present study, we examined the effects of prenatal lanthanum chloride exposure on memory consolidation using one-trial passive avoidance learning task in day-old chicks. The data suggest that chicks injected with lanthanum chloride (2 mg/kg) daily from E9 to E16 had significantly impaired long-term memory at 120 min after training (p < 0.05) but not the chicks injected with lanthanum chloride (0.1 mg/kg) daily from E9 to E16.     

Detour behaviour in horses (<Emphasis Type="Italic">Equus caballus</Emphasis>)

The objective of this study was to investigate the ability of horses (Equus caballus) to detour around symmetric and asymmetric obstacles. Ten female Italian saddle horses were each used in three detour tasks. In the first task, the ability to detour around a symmetrical obstacle was evaluated; in the second and third tasks subjects were required to perform a detour around an asymmetrical obstacle with two different degrees of asymmetry. The direction chosen to move around the obstacle and time required to make the detour were recorded. The results suggest that horses have the spatial abilities required to perform detour tasks with both symmetric and asymmetric obstacles. The strategy used to perform the task varied between subjects. For five horses, lateralized behaviour was observed when detouring the obstacle; this was consistently in one direction (three on the left and two on the right). For these horses, no evidence of spatial learning or reasoning was found. The other five horses did not solve this task in a lateralized manner, and a trend towards decreasing lateralization was observed as asymmetry, and hence task difficulty, increased. These non-lateralized horses may have higher spatial reasoning abilities.     

Evidence for hippocampal role in place avoidance other than merely memory storage

Spatial navigation is used as a popular animal model of higher cognitive functions in people. The data suggest that the hippocampus is important for both storing spatial memories and for performing spatial computations necessary for navigation. Animals use multiple behavioral strategies to solve spatial tasks often using multiple memory systems. We investigated how inactivation of the rat hippocampus affects performance in a place avoidance task to determine if the role of the hippocampus in this task could be attributed to memory storage/retrieval or to the computations needed for navigation. Injecting tetrodotoxin (TTX) into both hippocampi impaired conditioned place avoidance, but after injecting only one hippocampus, the rats learned the place avoidance as well as without any injections. Retention of the place avoidance learned with one hippocampus was not impaired when the injection was switched to the hippocampus that had not been injected during learning. The result suggests that during learning, the hippocampus did not store the place avoidance 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.     

Taking the Operant Paradigm into the Field: Associative Learning in Wild Great Tits

Associative learning is essential for resource acquisition, predator avoidance and reproduction in a wide diversity of species, and is therefore a key target for evolutionary and comparative cognition research. Automated operant devices can greatly enhance the study of associative learning and yet their use has been mainly restricted to laboratory conditions. We developed a portable, weatherproof, battery-operated operant device and conducted the first fully automated colour-associative learning experiment using free-ranging individuals in the wild. We used the device to run a colour discrimination task in a monitored population of tits (Paridae). Over two winter months, 80 individuals from four species recorded a total of 5,128 trials. Great tits (Parus major) were more likely than other species to visit the devices and engage in trials, but there were no sex or personality biases in the sample of great tits landing at the devices and registering key pecks. Juveniles were more likely than adults to visit the devices and to register trials. Individuals that were successful at solving a novel technical problem in captivity (lever-pulling) learned faster than non-solvers when at the operant devices in the wild, suggesting cross-contextual consistency in learning performance in very different tasks. There was no significant effect of personality or sex on learning rate, but juveniles’ choice accuracy tended to improve at a faster rate than adults. We discuss how customisable automated operant devices, such as the one described here, could prove to be a powerful tool in evolutionary ecology studies of cognitive traits, especially among inquisitive species such as great tits.