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

ELSEVIER

BEHAVIOURAL BRAIN RESEARCH Behavioural Brain Research 74 (1996) 153-159

Research report

Development of food-storing and the hippocampus in juvenile marsh tits

(Parus palustris) N.S. Clayton * Department of Zoology, Oxford University, South Parks Road, Oxford, OXI 3PS, UK Received 2 January 1995; revised 7 March 1995; accepted 7 March 1995

Abstract 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 day 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. Keywords: Avian hippocampus; Food-storing; Memory; Ontogeny

1. Introduction Some species of birds and mammals hide food and rely on an accurate and long-lasting spatial m e m o r y to retrieve their caches (e.g., [35,43]). Evidence that the avian hippocampus plays a role in m e m o r y for cache sites comes from two sources. Firstly, comparative studies have shown that food-storing birds have an enlarged hippocampus [23,37]. Secondly, birds with hippocampal lesions continue to store food but search randomly for their caches [25,38], which implies that the hippocampus plays a role in memory-based retrieval rather than in the behaviour of food storing per se. * Corresponding author. Present address: Division of Biological Sciences, Section of Neurobiology, Phsiology and Behavior, University of California, Davis, CA 95616-8519, USA. 0000-0000/96/$09.50 © 1996 Elsevier Science B.V. All rights reserved SSDI 0166-4328(95)00049-6

H i p p o c a m p a l damage also disrupts other forms of spatial m e m o r y in food-storing species [38], suggesting a functional similarity to the m a m m a l i a n hippocampus [28], which is thought to be homologous with the avian hippocampus [6,14,24,27,33], although the two are structurally distinct. In accord with the nomenclature of classical avian neuroanatomy [1,11,41], the term 'hippocampus' is used, short for hippocampal formation or hippocampal region, to indicate that both the hippocampus proper and parahippocampus are included. The correlation between food-storing and hippocampal volume, relative to brain and body size, is evident in comparisons of both diverse families of birds [23,37] and closely related species that engage in different amounts of food-storing [3,17,19,20]. Relative hippocampal volume is correlated positively with the number and/or importance of food caches typical of the species.

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A large hippocampus, relative to telencephalon and body size, is thought to reflect the increased demands on visuospatial cognition that may accompany scatterhoarding of food. This relationship is thought to be an example of a more general correlation between hippocampal volume and the importance of visuospatial cognition in the wild which occurs in several avian and mammalian species [39,40]. Species differences in hippocampal volume arise at a relatively late stage in development, after the young birds have fledged from the nest [18,21]. Recent work on the development of food-storing behaviour, memory and hippocampal anatomy in hand-raised marsh tits, Parus palustris [7-10] suggests that relative hippocampal growth is associated with some aspect of the memory experiences involved in food-storing behaviour or memory for previously encountered food [9]. In a series of experiments, hand-raised marsh tits were provided with, or deprived of, the opportunity to store food until different ages and the volume of the hippocampus was measured after different amounts of deprivation and/or experience [7,8,10]. The results of these studies suggest that the onset in food-storing behaviour begins at nutritional independence (day 35), that there is a sharp increase in the number of seeds stored at day 44 and that memorybased retrieval performance increases gradually after the onset in food-storing [8]. Other changes in food-storing behaviour, such as an increase in the length of time over which caches are left before retrieval, occur rapidly over a period of 10 days [7] which is consistent with reports of food-storing in juvenile tits in the wild [ 16]. The experience of storing and retrieving results in an increase in hippocampal volume, whilst absence of experience leads to attrition of hippocampal volume. These volumetric changes occur rapidly, over a period of 22 days, and are accompanied by increases and decreases respectively in cell number, suggesting that one effect of experience is to trigger recruitment of neurons, while the lack of experience may cause cell loss [10]. The effects were specific in the sense that they affected growth of the hippocampus but not growth of a 'control' area, the ectostriatum, or the telencephalon as a whole [9,10]. The aim of this experiment is to determine more precisely when the hippocampal growth occurs in relation to the behavioural development of food-storing. Greenough et al. have proposed two different types of mechanism which could trigger volumetric changes in the brain in association with cognitive demands [15]. The 'experience-expectant' hypothesis is that the brain would change in preparation for changes in cognitive demands, just as lengthening photoperiods results in changes in the gonads before breeding. The alternative 'experience-dependent' hypothesis is that specific areas of the brain may change in response to the experience of

new cognitive demands, in the same way as weight training may result in increased musculature of specific regions of the body. In this experiment, hand-raised marsh tits were given trials every third day in which they were provided with the opportunity to store and retrieve food and the volume of the hippocampus was measured after different amounts of experience and compared with those of age-matched controls. Some experienced and control birds were killed after eight trials (day 56) when differences between experienced and control birds in hippocampal volume should be apparent and some birds were killed at day 35 before the species differences in hippocampal volume emerge [ 10]. To test whether hippocampal growth precedes or accompanies changes in food-storing behaviour, other birds were killed after the third or fifth trial, one trial before (day 41) or one trial after (day 47) the sudden increase in food-storing and associated increased demands on memory-based retrieval of caches at day 44 [8]. The prediction from the first hypothesis that hippocampal growth precedes the sudden increase in food-storing is that experienced birds should have larger relative hippocampal volumes than age-matched controls at all three stages of the experiment. The alternative hypothesis is that changes in brain accompany or follow the changes in food-storing behaviour. In this case, experienced birds should not differ from controls before the fourth trial (day 44). Furthermore, given the role of the hippocampus in memory-based retrieval rather than the act of storing food I-9,25, 38 ], it is predicted that hippocampal growth in experienced birds would occur gradually in parallel with the gradual improvement in memory-based retrieval.

2. Materials and methods 2.1. Birds, groups and housing conditions

The subjects were 11 male and 10 female hand-raised, post-fledging juvenile marsh tits which were taken from Wytham woods under licence from English Nature. The juveniles were taken at day 12 post-hatch as half broods from seven marsh tit clutches and hand-raised until day 35 (nutritional independence). They were housed individually indoors in wire cages measuring 0.44 m wide x 0.99 m long x 0.44 m high and divided into groups. Each group received either 'Experienced' or 'Control' trials from day 35. On experienced trials, birds were allowed to store and retrieve the caches that they had stored; on control trials, birds received the equivalent amount of time in the room but were not allowed to store or retrieve. Three experienced (E) and three control (C) birds were killed after the third (day 41; E group, 2 males, 1 female; C group, 1 male, 2 females), fifth (day 47; E group, 3 females; C group, 2 males, 1 female) and

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eighth trial (day 56; E group 2 males, 1 female; C group, 3 males). In addition three birds were killed at the start of the experiment (day 35; 1 male, 2 females).

2.2. Experimental environment Throughout the experiment the birds were housed on a 10:14 light/dark cycle. Birds were deprived of food at 19:00 h and tested individually the following morning for their ability to store and remember the locations of these seeds. The experimental room was 3.5 x 2.0 × 2.8 m high and contained four 'trees' supported in plastic basins on the floor and a wooden stool containing water and a bowl of sunflower seeds. On every tree there were eight, individually numbered storage sites, with a wooden perch 5 mm below each hole. These were placed at regular intervals on the slanting faces of each tree for ease of perching. Each of the 32 storage sites was 5 mm diam. x 5 mm deep, just large enough for one seed, and was covered by a string knot to ensure that the birds could not see their caches.

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2.4. Neuroanatomical preparations Brains were treated in an identical way to control for effects of shrinkage. At the end of the experiment, birds were given a lethal intraperitoneal overdose of sodium pentabarbitone and perfused transcardially with heparinised physiological saline followed by 4% paraformaldehyde fixative. The brains were post-fixed in 4% paraformaldehyde for 7 days. The brains were cut as 6 gm coronal sections that had been embedded in paraffin. Every tenth section was stained with cresyl violet. The volume of the hippocampal region (whose boundaries have been defined previously using a combination of techniques (e.g., [ 14,23,24,37-39]) and the remainder of the telencephalon were traced from the sections using a 10 x photographic enlarger. The traced outlines were measured using a W A C O M @ graphics tablet and Image 1.51@, and the volumes of the hippocampus and telencephalon (minus hippocampus) were computed using the formula for a truncated cone [9,10,21]. All measurements were done blind.

3. Results

2.3. Experimental protocol 3.1. Development offood-storing behaviour Each trial consisted of two phases. In 'experienced' trials, the bird was provided with a bowl containing dehusked sunflower seeds in phase I and allowed to store for 20 min. After a retention interval of 2 h, which the bird spent in its home-cage, it was allowed back into the room for 10 min during a second phase in which birds could search for their caches. Birds receiving 'control' trials were treated in an identical way except that they were given powdered sunflower seed which they could eat but not store in phase I; in phase II, control birds flew and perched in the room but did not retrieve because they had not cached seeds. All birds were given one seed in their homecage after every trial to ensure that control birds had some experience in handling seeds during the experiment. To ensure that all birds were familiar with the storing environment prior to the experiment, all birds were given exposure to seeds and the testing room for 5 days before the experiment started (day 30-34). The number of seeds stored in phase I, the number of seeds retrieved in phase II, and the number of visits to the storage sites (looks) in phase I and II of each trial were recorded for each bird. A seed was recorded as having been stored if it remained in the storage site at the end of the storing phase. Tentative attempts at storing, in which the stored seed was retrieved and then dropped or eaten before the end of the storing trial, were not counted. A bird was said to have made a look when it pulled at the string covering one of the 32 potential storage sites.

The mean and standard errors of the number of seeds stored and retrieved over the 8 trials are shown in Fig. 1. There was a significant increase in the number of seeds stored over the eight trials (linear regression: y = - 0 . 2 9 5 + 0 . 9 0 x , r2=0.90, F1,6=51.60 , P<0.001) and there was a sharp increase between trial 3 and 4. A oneway analysis of variance with trial as a repeated measure on the no. seeds stored by the three experienced birds that completed all eight trials showed a significant effect of trial (F9,18=19.949, P<0.001) and post hoc tests 6" •

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revealed that the main difference is between trial 3 and 4 (Duncan New Multiple Range, P <0.05). The number of seeds that were retrieved per trial increased gradually over the first few trials in which the birds were storing several seeds (linear regression: y = -0.24+0.54 x, r 2 =0.92, E l , 6 =69.90, P<0.002). Fig. 2 shows that in later trials birds make fewer incorrect looks before finding each seed. Birds consistently make more looks during phase II than the number of seeds that they had stored and there is no significant difference between trials in the number of looks per trial (repeated measures one-way analysis of variance, P>0.05). This suggests that the increase in number of seeds that were retrieved per given number of looks is not simply a consequence of the increase in the number of seeds stored per trial but that there is an increase in the proportion of successful retrievals in later trials. One way analyses of variance with sex as the independent variable and number of seeds stored and retrieved as the independent variable respectively, showed that there was no significant effect of sex (P > 0.05 in both cases).

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Vol Telencephalon(mm3) Fig. 3. Hippocampal volume plotted against telencephalon volume (mm 3) for experienced birds which received food-storing and retrieval trials and age-matched controls which received an equivalent amount of time in the food-storing arena but were prevented from storing and retrieving caches. Three birds were killed for neuroanatomical work at day 35 prior to the experiment. Three experienced birds (open symbols) and three control birds (filled symbols) were killed after trial 3 (day 41), trial 5 (day 47) and trial 8 (day 56), respectively. See Fig. 1 legend and text for further details.

alon volume the residuals of hippocampal volume on telencephalon volume were analysed by an analysis of variance with relative hippocampal volume as the dependent variable and treatment groups as the independent variable on all 21 birds. There was a significant effect of t r e a t m e n t ( F r A 8 = 9.90, P < 0.001) and post-hoc comparisons using Duncan New Multiple Range (P < 0.05) show that the difference arises because pre-experiment birds and those in all three control groups have significantly smaller relative hippocampal volumes than those in all three experienced groups which were killed at the same age (Fig. 4). There were no significant differences between the sexes in any of the three brain volume measures (one-way analysis of variance with sex as the independent variable, P > 0.05 in each case). To test for the effects of stage of the experiment versus food-storing experience on brains of the 18 birds that took part in the food-storing experiment, three two-way

3.2. Developmentof the hippocampus The results of the volumetric analysis of the brains are illustrated in Fig. 3 which shows hippocampal volume plotted against telencephalon volume. Brain volume measurements were logarithmically transformed to normalise the data. A stepwise multiple regression with hippocampal volume as the dependent variable and telencephalon volume and body weight as the independent variables showed that there was a significant association between telencephalon and hippocampal volume (r2=0.40, Fm9=18.30, P<0.01) and but not between body weight and telencephalon (r2 = 0.005, Fl,19 = 0.10, P<0.99) or body weight and hippocampal volume (r2 = 0 . 0 0 5 , FI,19 =0.90, P=0.35). To test whether or not the groups showed significant differences in hippocampal volume relative to telenceph-

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analyses of variance were carried out on log hippocampal volume, log telencephalon volume and relative hippocampal volume respectively with stage of the experiment (killed after trial 3, 5, 8) and treatment (experience versus control) as the independent variables in each case. There was a significant effect of stage (F2,12=6.30, P<0.01) and treatment (FL12 = 32.40, P < 0.001) on log hippocampal volume but no significant effect of interaction (F2,i2=0.20, P=0.81). For log telencephalon volume, there was a significant effect of stage (F2,12=5.40, P < 0.02) but neither treatment (Fro2 = 1.9, P = 0.98) nor interaction (F2,12=0.02, P=0.89) reached significance, whereas for relative hippocampal volume treatment had a significant effect (F1,12=36.80, P<0.001) but stage (F1,12=0.30, P=0.99) and interaction terms were not significant (F2,i2=0.10, P=0.89). It can be seen from Fig. 3 that telencephalon and hippocampus increase in volume over the three stages of the experiment for both experienced and control birds but that there is an additional increase in hippocampal volume seen in the experienced groups. Comparing the absolute and relative hippocampal volumes of the birds in the three experienced groups showed that there was a significant association between the absolute volume of the hippocampus and total number of seeds stored ( y = 1.1 +0.0065 z, r 2=0.4,F~,9=5.5, P<0.05) and retrieved ( y = 1.1+0.0094x, ra=0.5, F1,9=5.8, P<0.05) but not in the total number of looks made in phase I or phase II (P > 0.05 in each case). However, these differences arose because of the effect of stage of the experiment on hippocampal volume. Within each stage, there was no significant association between the absolute volume of the hippocampus and total number of seeds stored and retrieved (P > 0.05 in each case). Furthermore, for absolute telencephalon volume and relative hippocampal volume the associations between brain volume and number of looks made in phase I and II, and the total number of seeds stored and retrieved were not significant (P > 0.05 in each case).

4. Discussion

The main results can be summarised as follows. (1) Experienced birds showed a sharp increase in the number of seeds stored at day 44 while the proportion of successful retrievals improved gradually after the onset of food-storing, confirming the observations reported by Clayton [8]. (2) There was a significant effect of treatment: experienced birds had larger absolute and relative hippocampal volumes than did controls at all three stages of the experiment. There was no statistical difference in telencephalon volume of experienced and control birds. (3) The stage at which the birds were killed had a significant effect on the absolute volume of both the

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hippocampus and telencephalon (minus hippocampus) but not on relative hippocampal volume. (4) There was no significant interaction between the effect of treatment by stage at which the birds were killed. The neuroanatomical findings are consistent with those of two previous studies which showed that some aspect of food-storing experience [10] or memory for previously encountered food triggers growth of the hippocampus [9]. However, the results also provide more detail about when the changes in brain occur. The results of this study show that both the telencephalon and hippocampus increase in volume over the three stages of the experiment for both experienced and control birds, suggesting that this growth maybe a result of maturation or increased general experience such as flying around the room. However, there is an additional increase in hippocampal volume, which is found only in the experienced groups, suggesting that the additional growth of the hippocampus may be associated specifically with some aspect of storing and retrieving seeds. Within the three experienced groups killed after three, five and eight trials, respectively, there is no statistically significant difference between the three stages in relative hippocampal volume, and no significant association between relative hippocampal growth and the total number of seeds stored and retrieved by each bird in the experienced groups. These findings support the results of Clayton and Krebs [ 10] who reported that, above a certain level, cumulative experience has no further effect on relative hippocampal growth. The results of this study suggest that the additional hippocampal growth found only in experienced birds occurs at an early stage in the development of foodstoring behaviour, before the sharp increase in foodstoring intensity on day 44 and associated increased demands on memory for cache sites. These results may be taken to support the first hypothesis that growth of the hippocampus occurs in preparation for food-storing rather than accompanying or following the changes in food-storing. However, one needs to explain why the hippocampal growth is not found in controls. 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. Alternatively, the presence of ad lib. whole seeds or the opportunity to store and retrieve trigger the increase in hippocampal volume. It is also possible that some other difference between the experienced and control trials, that is not directly related to some aspect of food-storing or memory-based retrieval, results in the increase in hippocampal volume of experienced birds. In terms of visual stimulation, motor experience and diet, the control and experienced birds were as nearly as possible identical: control birds were allowed to enter the same food storing arena for the same amount of time on each trial as the experienced birds, but they were given powdered seed

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which they could not store. Thus, it seems unlikely that the differences in hippocampal volume of controls and experienced birds could be accounted for in terms of a general deprivation versus enrichment effect. Furthermore, it is important to note that there was no significant correlation between any of the three brain volume measurements and the number of looks made in phase I and II. Given that hippocampal lesions disrupt memory-based retrieval and not food-storing per se, the results suggest that hippocampal growth in experienced birds may be directly related to the increased ability to remember the locations of caches, rather than an increase in the motivation to store food or search for cache sites. Several studies have shown that the developing brain of both birds and mammals, including the mammalian hippocampal region, can change in response to certain kinds of sensory input or experience and to hormonal influences [ 12,13,15,22, 29,30, 32, 34], but the closest parallel with the present results comes from the song system of passerine birds where developmental changes in the volumes and neuron numbers of some of the song control nuclei such as lateral MAN, an area involved in early memorisation of songs, occur before the bird acquires a fully developed song. These changes were interpreted originally as being linked directly with song learning [29]. However subsequent work suggests that these changes in the brain precede song learning and are independent of auditory experience [5]. Another common feature of both food-storing and the song system is that behaviour shows a seasonal cycle. Observations in both the laboratory and field suggest that food-storing behaviour is more marked in the autumn and winter than in the spring and early summer (e.g., [26,31,36]), although some storing behaviour persists throughout the year. The results of this study therefore raise the possibility that older experienced birds may respond to food-storing experience in the same way each Autumn. Recent work suggests that the hippocampus may also change seasonally [2,42], although the results to date are equivocal and it is unclear whether the changes are linked to food-storing or reflect a more general seasonal effect [36]. In the song control nuclei, seasonal changes [30] are associated with seasonal alterations in singing but they appear to be an effect of more general seasonal changes which results from altered levels of circulating steroid hormones associated with reproduction rather than as a direct result of changes in singing [4]. The present results suggest that the avian hippocampal region of food-storing birds is a useful model for investigating how specific types of experience trigger changes in volume of specific regions of the brain but more detailed investigations of the neural activity of the hippocampus are required to determine exactly how and what kinds of experience influence hippocampal growth.

Acknowledgment This work was supported by a BBSRC grant and fellowship. Thanks to Sanjay Patel, Jenny Corrigan, Nick Lewis, Anna Jolliffe, David Wilson for technical assistance and to Anna Jolliffe, Diane Lee, Sanjay Patel and Sara Shettleworth for comments on the manuscript.

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