Nicky S. Clayton

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 learning induces neurogenesis in the avian brain

It is known from previous work that neurones are born continuously in the ventricular zone of the bird brain. In this study, we show that the amount of cell proliferation in the ventricular zone of the hippocampus (HP) and the hyperstriatum ventrale (HV) is influenced by behavioural experience. Two groups of birds (marsh tits) were compared: those allowed to store and retrieve food once every 3 days between days 35 and 56, and age-matched controls treated in an identical way, except that they were not allowed to store and retrieve food. After three trials of storing and retrieval, between days 35 and 41 posthatch, experienced birds showed a significantly higher rate of cell proliferation than did controls. The experienced birds also showed a significant increase in total cell and neuronal number by day 56 posthatch, after eight trials of storing and retrieval. There were no significant differences in the amount of programmed cell death in the hippocampus in this study. In a novel analysis of the data we demonstrate that the effect of experience between days 35 and 41 was to increase the daily rate of neurogenesis in the ventricular zone from 3.9 to 10%, and that this change could account for the increase in total hippocampal neuronal number by day 56 in the experienced birds. Thus, the observed increase in hippocampal volume and neuronal number as a result of food storing and retrieval, may be caused by an increase in neurogenesis in the first few trials of food storing experience.

Memory in food-storing birds: from behaviour to brain

As a result of natural history studies, it has been hypothesized that food-storing birds may develop a special kind of memory to cope with the demand imposed by their food-storing behaviour (i.e. the ability to retrieve food from a wide variety of stores over varying amounts of time after storage). Recent studies on food-storing birds suggest that, at a relatively late stage in their development, the specific memories associated with food-storing behaviour can stimulate growth of the hippocampus, an area of the brain concerned with memory processing.

Development of memory and the hippocampus: comparison of food-storing and nonstoring birds on a one-trial associative memory task

Food-storing birds, for example, marsh tits, Parus palustris, use memory to retrieve stored food and have a larger hippocampus relative to the rest of the telencephalon than do species that store little or no food such as the blue tit, P. caeruleus. The difference between food storers and nonstorers in relative hippocampal volume occurs after the young birds have fledged from the nest and is dependent upon some aspect of memory for retrieving caches of stored food. To test whether or not species differences in memory and volumetric changes in the hippocampus could be triggered by experience of memory tasks other than retrieval of stored food, groups of hand-raised marsh tits and blue tits were tested between days 35 and 192 posthatch on a one-trial associative memory task in which they were rewarded in phase II for returning to the feeder where they had eaten part of a peanut 20 min earlier. No species differences were found when the peanut was visible in phase I, but when the peanut was hidden in phase I, marsh tits performed better than blue tits, irrespective of whether or not they had had previous experience of storing and retrieving food. In dissociation trials (transformed array of feeders), marsh tits with food-storing experience responded preferentially to spatial cues, whereas blue tits responded equally to both spatial position and object- specific cues. These species differences are also found in wild-caught adults. However, marsh tits without food-storing experience responded equally to both spatial position and object-specific cues, which suggests that experience of storing and/or retrieving caches is required in order for marsh tits to develop the spatial preference seen in adult food storers. Both marsh tits with experience of the one-trial associative memory task and those that had also had food-storing experience had larger relative hippocampal volumes than did controls, independent of age. Of the marsh tits trained on the one-trial associative memory task, there was no difference between those that had had food-storing experience and those that had not. However, in blue tits, there was no effect of experience on relative hippocampal volume. No volumetric differences were observed in ectostriatum, which served as a control brain region. The results suggest that some aspect of memory for retrieving food (whether or not stored by the bird) directly influences growth of the hippocampal region in marsh tits, the food- storing species, but not in blue tits, the nonstoring species.

Development of hippocampal specialisation in two species of tit (Parus spp.)

Food storing birds have been shown to have a larger hippocampus, relative to the rest of the telencephalon, than do non-storers. A previous study reported that this difference in relative hippocampal volume is not apparent in a comparison of nestling birds, but emerges after birds have fledged. This conclusion was based on a comparison of a storing and a non-storing species in the corvid family. The present study compared another storer/non-storer pair of species in order to test whether the results of the previous study can be replicated in another family of birds. The volumes of the hippocampal region and remainder of the telencephalon were measured and estimates of neuron size, density and total number in the hippocampal region were made for nestlings and adults of the food-storing marsh tit Parus palustris and non-storing blue tit Parus caeruleus. Relative hippocampal volume did not differ between nestlings of the two species, whilst the relative hippocampal volume of adult marsh tits was greater than that of blue tits. The difference between adults arose because in marsh tits but not blue tits, adults had a significantly larger relative hippocampal volume than did nestlings. Neuron density was significantly higher in both species in nestlings than in adults and adult blue tits had fewer neurons than did adult marsh tits. The results of this study are largely consistent with the earlier study comparing a storing and non-storing species of corvid, suggesting that the observed patterns may reflect a general difference between storers and non-storers in the development of the hippocampal region.

Lateralization and unilateral transfer of spatial memory in marsh tits

SummaryThe results reported in this paper demonstrate lateralization and transfer of spatial memory processing in an adult, food-storig bird. The technique of monocular occlusion was used to investigate lateralization and memory transfer in food-storing marsh tits (Parus palustris) for two tasks, food-storing and one-trial associative learning, which rely on one-trial learning for the spatial location of hidden food items. In the food-storing task, marsh tits had to return to the sites where they had previously stored a seed; in the one-trial associative learning task, the birds had to return to sites where they had been allowed to eat some, but not all, of a piece of peanut. For both spatial memory tasks, it was demonstrated that although the visual systems fed by both eyes are involved in short-term storage, the right eye system is associated with long-term storage, and that memories are transferred from the left to the right eye system between 3 and 24 h after memory formation.

One-trial associative memory: Comparison of food-storing and nonstoring species of birds.

Experiment 1 compared food-storing marsh tits and nonstoring blue tits, and Experiment 2 compared food-storing jays and nonstoring jackdaws, in a one-trial associative memory task, Birds obtained a reward by returning to the site where they had eaten part of the reward 30 min earlier. In “visible” versions, the reward was visible in Phase 1 but hidden in Phase 2 so that the bird had to search for it; in “hidden” versions, the reward was hidden in both phases. No species differences were found in performance in the visible version. However, in the hidden version, the 2 storers preferentially returned to rewarded sites, whereas nonstorers preferentially returned to sites that had been visited in Phase 1, irrespective of whether or not they contained a reward. This suggests that storers differ from nonstorers in the way they discriminate between remembered events.

Development of food-storing and the hippocampus in juvenile marsh tits (Parus palustris).

Food-storing birds, e.g., marsh tits, Parus palustris, use memory to retrieve stored food and have a larger hippocampus relative to the rest of the telencephalon than do species that store little or no food, e.g., blue tits, P. caeruleus. The difference in relative hippocampal volume arises after the young have fledged from the nest and recent work on the dual ontogeny of the hippocampus and memory in hand-raised marsh tits suggests that the hippocampal growth depends upon some aspect of the experience of storing and retrieving food. The aim of this experiment was to test whether hippocampal growth precedes or accompanies changes in food-storing behaviour. Hand-raised marsh tits were provided with the opportunity to store and retrieve food every third day from day 35 post-hatch and the volume of the hippocampus and remainder of the telencephalon was measured and compared with those of age-matched controls at three different stages (days 41, 47 and 56 post-hatch). Experience had no significant effect on telencephalon volume but experienced birds had larger absolute and relative hippocampal volumes than did controls at all stages of the experiment, even before the increase in food-storing intensity on day 44. The stage at which the birds were killed had a significant effect on the absolute volume of both the hippocampus and telencephalon but there was no significant interaction between experience and stage. The results suggest that both hippocampus and telencephalon continue to increase in volume between days 35 and 56 but that the hippocampus shows a additional increase in volume relative to telencephalon in the experienced groups. One interpretation of these results is that the one or two seeds stored before day 44 may have been sufficient to stimulate the growth of the hippocampus and that there is an increase in relative hippocampal volume in preparation for the increased memory demands associated with the sharp increase in food-storing.

Lateralization in Paridae: comparison of a storing and a non-storing species on a one-trial associative memory task

SummaryWe 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.

The neuroethological development of food-storing memory : a case of use it, or lose it !

Some species of birds that scatter-hoard food e.g. marsh tits, Parus palustris, use memory to retrieve stored food. These scatter-hoarding species have a larger hippocampus relative to the rest of the telencephalon than do species that store little or no food e.g. blue tits, P. caeruleus. The difference in relative hippocampal volume arises after the young have fledged from the nest and recent work on the dual ontogeny of the hippocampus and memory in hand-raised marsh tits suggests that some aspect of memory for retrieving food (whether or not stored by the bird) can stimulate hippocampal growth in juveniles at a relatively late stage in their development.