Migratory behavior, spatial memory and the hippocampus

Memory is an important mechanism by which all animals acquire and retain information about the surrounding world and is essential for existence and survival. In order to understand how memory operates it is crucial to understand how it is related to the underlying neural mechanisms and which factors could have shaped the evolution of memory and the underlying mechanisms.

Much research on the relationship between environment, memory and the hippocampus has been focused on food-caching birds which use memory to recover numerous food caches. It appears that food-caching specialization has resulted in enhanced spatial memory and an enlarged hippocampus in both birds and mammals even though this topic remains highly controversial (Bolhuis & Macphail 2001; Macphail & Bolhuis 2001).

Whereas food-caching birds is a great model to investigate whether higher demands for better memory might result in enhanced memory and an enlarged hippocampus, it is crucial to investigate alternative models. Alternative models might provide more evidence about the generality of the relationship between environmental demands for better memory, memory and the hippocampus. One of such alternative models is migratory birds. Many avian species regularly migrate thousands of miles every year between breeding and wintering grounds and it has been suggested that migratory birds need to use a complex navigational system in which learning and memory should be an important component (Mettke-Hofmann & Gwinner 2003). Long-distance migrants might need to remember their migration route, stopover sites required for refueling energy reserves and which appear to be used over many years and the details of both breeding and wintering habitats, as both habitats seem to be re-used. Hippocampus-dependent memory also appears to be important for fine-tuned homing (Strasser et al. 1998).  It has been suggested that whereas young migratory birds are likely to use a simple “vector navigation” system, older birds use a more complex orientation system based on memory and learning (Mettke-Hofmann et al. 2003).

If migratory species indeed have higher demands for memory they might be expected to have enhanced memory and an enlarged hippocampus compared to non-migratory species. Two alternative hypotheses might explain potential differences between migratory and non-migratory birds in memory and hippocampal size. First, it is possible that migratory experience per se triggers these changes (Healy et al. 1991). Second, migratory birds might have enhanced memory and an enlarged hippocampus as a result of increased selection pressure for better memory needed for successful migration (Cristol et al. 2003).

Very little information is available on memory and the hippocampus of migratory and non-migratory birds and a few available studies provide some support to the hypothesis that migratory life style may affect memory and the hippocampus (Healy et al. 1991; Cristol et al. 2003; Mettke-Hofmann & Gwinner 2003). Healy et al. (1991) reported that relative hippocampal volume and the total number of neurons in migratory garden warblers (Sylvia borin) increases after migratory experience. In non-migratory Sardinian warblers (Sylvia melanocephala), on the other hand, there were no differences between adult and juvenile individuals in absolute hippocampal volume (Healy et al. (1991). Young migratory garden warblers that were prevented from migration for a year had significantly smaller hippocampus and fewer neurons compared to the birds that experienced migration supporting the first hypothesis that migration experience directly affects hippocampal volume and the total number of neurons (Healy et al. 1991). However, no comparison between migratory garden warblers and non-migratory Sardinian warblers were presented and data on memory performance were also not available.

Cristol et al. (2003) reported that migratory subspecies of dark-eyed juncos (Junco hyemalis hyemalis) showed better memory performance in laboratory conditions and had higher density of hippocampal neurons compared to non-migratory juncos (J. h. carolinensis). Migratory and non-migratory juncos did not differ in their hippocampal volume and the total number of hippocampal neurons was not presented or analyzed. Results of Cristol et al. (2003) support the general hypothesis that migratory birds should have better memory but they do not differentiate between the alternative hypotheses about the origin of such differences.

Finally, Mettke-Hofmann & Gwinner (2003) compared long-term memory of migratory garden warblers and non-migratory Sardinian warblers and reported that migratory warblers showed better memory performance. Unfortunately, Mettke-Hofmann & Gwinner (2003) did not investigate the hippocampal structure of their birds and referred to the previous study (Healy et al. 1996), which actually did not compare relative hippocampal volume and the total number of neurons between these two species.

Although all three studies provided some support to the hypothesis that migratory behavior results in enhanced spatial memory and an enlarged hippocampus, the results are not clear. Healy et al. (1996) showed that migratory experience triggered an increase in relative hippocampal volume and in the total neuron numbers in a migratory species but it remained unknown whether memory was affected by migratory experience and whether a migratory species had better memory and larger hippocampus than a non-migratory species. Healy et al. (1996) used relative hippocampal volume in their comparison of experienced and naïve migratory garden warblers but absolute hippocampal volume when comparing non-migratory adult and juvenile Sardinian warblers. Data presented in Healy et al. (1996), on the other hand, suggest that relative hippocampal volume is also different between adult and juvenile Sardinian warblers.  Cristol et al. (2003) found differences in memory and in hippocampal neuron density but not in the hippocampal volume between migratory and non-migratory birds. Mettke-Hofmann & Gwinner (2003) found differences in long-term memory between migratory and non-migratory species but it remains unclear whether these differences were related to any differences in the hippocampal structure and it also remains unclear what kind of memory was affected by migratory behavior. Data in Healy et al. (1996) actually suggest that relative hippocampal volume of garden and Sardinian warblers is similar and that relative hippocampal volume of adult Sardinian warblers is larger than that of juvenile warblers. Thus, available studies do not provide sufficient evidence that all three components - migratory behavior, memory and the hippocampus are related.

We have been investigating the relationship between migratory experience, memory and the hippocampus using the white-crowned sparrow (Zonotrichia leucophrys). There are several subspecies of the white-crowned sparrow and two of these appear to be drastically different mainly in one component of their biology, which is most likely to provide high demands for spatial memory – long distance migration (Mewaldt et al. 1968; Chilton et al. 1995). Whereas Gambel’s white-crowned sparrows (Z. l. gambelii) are long-distance migrants breeding in Canada and Alaska and migrating every year to California for the winter (sometimes as far as 4,300 km), Nuttall’s white-crowned sparrows (Z. l. nuttalli) are sedentary and reside permanently in the same areas along California coastline during both summer and winter (Chilton et al. 1995). These two subspecies appear to represent an excellent model for testing the hypothesis that migration has an effect on memory and the hippocampus. Unlike the dark-eyed junco comparison (Cristol et al. 2003) in which even the non-migratory J. h. carolinensis might exhibit short-distance movements during the winter (Nolan et al. 2002), non-migratory Z. l. nuttalli appear to be truly resident throughout the year (Chilton et al. 1995). White-crowned sparrows are easy to separate into two age classes, first year juveniles and adults, based on their plumage coloration. First-year migratory birds captured on their wintering grounds in northern California have only completed their first one-way migration whereas adults have experienced at least two and a half way migration. In non-migratory sparrows, the main difference between adults and juveniles is in their age. Thus, if extensive migratory experience directly affects hippocampal structure we should be able to detect the differences in the hippocampus between adult and juvenile migratory sparrows but not in non-migratory species.

We have been specifically testing: (1) whether migratory sparrows show better memory performance than their non-migratory conspecifics; (2) whether migratory sparrows have larger hippocampus with more neurons than their non-migratory conspecifics and (3) whether there are differences between adult and juvenile sparrows. Whereas hippocampal size and neuron numbers are likely to affect spatial memory ability, memory performance might also be affected by the immediate levels of glucocorticoid hormones, and elevated corticosterone levels have been reported to enhance spatial memory performance in birds (Pravosudov 2003). Therefore, we also compared baseline and stress-induced corticosterone levels of migratory and non-migratory sparrows as a source for potential differences in memory performance.