A final line of evidence for the spatial function of the hippocampus comes from comparative studies. Passerine birds, breeds of domestic pigeons, and strains of mice all vary in their ability to perform spatial tasks. Among the passerines, most chickadees, tits, crows, jays, and nuthatches hoard food avidly (see chap. 7). These birds create thousands of scattered food caches and retrieve them primarily by remembering where they put their hoarded food (Kamil and Balda 1990; Sherry and Duff 1996; Shettleworth 1995). Lesions of the hippocampus disrupt accurate cache retrieval and selectively impair performance on spatial, but not nonspatial, tasks (Sherry and Vaccarino 1989; Hampton and Shettleworth 1996). Chickadees given an antagonist to the NMDA receptor (see section 3.4) were impaired in their ability to form long-term, but not short-term, spatial memories (Shiflett et al. 2004).
Food-hoarding birds have much larger hippocampi than do nonhoarding birds (Krebs et al. 1989, 1996; Sherry and Duff 1996; Sherry et al. 1989). Even within genera of food-hoarding birds, variation in the intensity of food hoarding correlates with the relative size of the hippocampus (Basil et al. 1996; Hampton et al. 1995; Healy and Krebs 1992; Lucas et al. 2004). Among strains of domestic pigeons, those with homing ability have a larger hippocampus than strains selected for other attributes (Rehkamper et al. 1988). Among strains of laboratory mice, those with the best scores on tests of spatial ability have more and longer neuronal projections running within the hippocampus from the dentate gyrus to the CA3 cell field (Schwegler and Lipp 1995).
In some species, males and females may be subjected to different selection pressures on spatial ability. As brood parasites, female brown-headed cow-birds, but not males, search for host nests in which to lay eggs. Females lay at dawn or earlier, probably in a nest they initially located between one and several days before. After laying, females spend the rest ofthe morning searching for host nests in which to lay subsequent eggs. They learn the locations of potential host nests and probably retain other information, such as the stage of completion ofthe nests they find. Female brown-headed cowbirds have a larger hippocampus than males, a sex difference not found in closely related icterid blackbirds that are not brood parasites (Sherry et al. 1993).
South American cowbirds exhibit wide variation in behavior that permits additional comparisons. The bay-winged cowbird is not a brood parasite. It usurps the nests of other birds, but incubates its own eggs and raises its own young. The bay-winged cowbird is, however, the sole host of a specialist parasite, the screaming cowbird. Screaming cowbird males and females search together for bay-winged cowbird nests. Another cowbird, the shiny cowbird, is a generalist brood parasite, and as in the generalist brown-headed cowbird of North America, female shiny cowbirds search for host nests without male aid. Reboreda et al. (1996) found a sex difference favoring females in the relative size of the hippocampus in the shiny cowbird, but not in the other two species, confirming that sex-specific selection can affect the size of the hippocampus in one sex but not the other.
The highly variable mating systems of Microtus voles provide a final comparative example of selection for spatial ability and its effects on the hippocampus. Meadow vole males are highly polygynous, and during breeding they occupy home ranges that encompass the home ranges ofmultiple females (Gaulin and FitzGerald 1986, 1988). These males, in effect, compete spatially for breeding opportunities (Spritzer, Meikle et al. 2005; Spritzer, Solomon et al. 2005). Pine voles, in contrast, are monogamous, and males and females occupy the same home range together. The hippocampus of male meadow voles is larger than that offemales, a sex difference not found in monogamous pine voles (Jacobs et al. 1990).
In these examples, variations in spatial ability correlate with differences in hippocampal size. The requirement for augmented spatial ability, and hence the need for a large hippocampus, also appears to vary seasonally in some animals. The hippocampus of food-hoarding birds, for example, varies in size seasonally in step with seasonal variation in food-hoarding activity. The hippocampus ofthe black-capped chickadee reaches a maximum size in October, at about the onset of seasonal food hoarding in this species. The hippocampus, surprisingly, decreases in size by December, even though food hoarding persists through the winter (Smulders et al. 1995).
Neurogenesis, the birth ofnew neurons, occurs in the chickadee hippocampus in a seasonal pattern that conforms to the seasonal patterns of change in hippocampal volume and food hoarding (Barnea and Nottebohm 1994, 1996). Incorporation ofnew neurons into the chickadee hippocampus reaches a peak in October, with relatively low neurogenesis at other times ofthe year. Why should fall maxima occur in both hippocampal volume and neuronal recruitment in black-capped chickadees? If these changes have anything to do with food hoarding, it would appear that the hippocampus undergoes changes that coincide with the onset ofhoarding, but increased hippocampal size and high rates ofneuronal recruitment do not persist through the winter, even though hoarding and retrieval of food continues for many months. It is not too surprising that a large hippocampus might not be maintained if it is not needed. Brains are energetically expensive to operate (Laughlin 2001). Smulders and colleagues (Smulders and DeVoogd 2000; Smulders and Dhondt 1997) suggest that the major demands on spatial ability may occur with the initial placement of caches in early fall. Chickadees space their caches widely to safeguard them from systematic pilfering by other animals. Smulders argues that memory for the spatial locations of caches is necessary for this spacing in the fall, but plays a lesser role in cache retrieval later in the winter. There are other possibilities, too. The fall peak in hippocampal size and neuronal recruitment may change the state ofthe hippocampus, enhancing memory in a way that persists throughout the winter or until the next phase ofvolume change and neuroge-nesis. A full understanding of the functional importance of seasonal changes in size and neurogenesis in the avian hippocampus requires a more complete account of how the hippocampus represents and processes information.
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