Hippocampus and memory for food caches in black-capped chickadees.

Abstract

Black-capped chickadees and other food-storing birds recover their scattered caches by remembering the spatial locations of cache sites. Bilateral hippocampal aspiration reduced the accuracy of cache recovery by chickadees to the chance rate, but it did not reduce the amount of caching or the number of attempts to recover caches. In a second experiment, hippocampal aspiration * dissociated performance of a task requiring memory for places from performance of a task requiring memory for cues associated with food, disrupting the former but not the latter. On both tasks, however, hippocmpal aspiration increased the frequency of revisiting errors to sites previously searched. These experiments show that the structure in the avian brain that is neuroanatomically and embryologically homologous to the mammalian hippocampus shares some functions with the mammalian hippocampus. The results indicate that memory for places and working memory are both disrupted by hippocampal damage in birds. Finally, it was possible to show that these memory capacities are essential for cache recovery by black-capped chickadees.Black-capped chickadees (Parus atricapillus) store food in concealed locations scattered throughout their home range. They store seeds and invertebrate prey, and they put each food item in a separate cache site. Hollow stems, crevices in bark, moss, leaf buds, dry leaves, and natural cavities are used as storage sites. Chickadees, and the congeneric marsh tit (Parus palustris), may store as many as several hundred food items per day and place neighboring caches at least several meters apart. They recover their stored food a few days after caching it, and in the wild they do not reuse cache sites Sherry, Avery, & Stevens, 1982;Stevens &Krebs, 1986). Stored food is recovered by remembering the spatial locations of caches (Cowie et al., 1981;Sherry, 1984a;Shettleworth & Krebs, 1982).The evidence that memory for spatial locations is the principal means of cache recovery comes from a number of experimental field and laboratory studies, reviewed by Sherry (1985). In the field, seeds are taken from cache sites at a higher rate than they are taken from identical control sites 10 cm away (Cowie et al., 1981). Although this is not unequivocal evidence of memory, it shows that cache recovery is spatially precise and is not based on exhaustive search of all sites resembling the cache site. An experiment in which This research was supported by the Natural Sciences and Engineering Research Council of Canada.We thank Alison Fleming, Michael Leon, Larry Squire, and Franco Vaccarino for their advice and encouragement, and Elisabeth Murray and Derek van der Kooy for their comments on an earlier draft of the manuscript. We are grateful to Karen Buckenham and Siegfried Schulte for their technical assistance and to Jim Hare for his help catching chickadees.

Blocking in landmark-based search in honeybees

“…Strong support for the distinction has been provided by studies showing that hippocampal lesions impair rats' ability to learn the new location of an invisible platform (locale learning) but not their ability to find a visible platform (guidance, or beacon learning; see, e.g., Morris, Garrud, Rawlins, & O'Keefe, 1982; for a review, see Leonard & McNaughton, 1990). An analogous effect is found in food-storing birds with hippocampal lesions (e.g., Sherry & Vaccarino, 1989), who have trouble remembering the location of stored caches of food, but can still learn to approach a particular cue. Given this distinction, guidance learning is reasonably expected to follow principles of Pavlovian conditioning, but locale learning might not (Morris, 1981).…”

Place and cue learning in turtles

“…For instance, in mammals and birds, damage to the hippocampal formation, which is considered homologous in both taxa on the basis of anatomical evidences (Bingman, 1992), produces selective impairments in spatial tasks that require the encoding of reciprocal relationships among environmental features (place learning), but not in tasks requiring the subject to approach a single cue or requiring non spatial discriminations (Bingman & Mench, 1990;Fremouw, Jackson-Smith, & Kesner, 1997;Good, 1987;Morris et aI., 1982;Nadel & MacDonald, 1980;Okaichi, 1987;Olton & Papas, 1979;Pearce, Roberts, & Good, 1998;Sherry & Vaccarino, 1989). However, a feature can be considered homologous in two or more taxa only if it can be traced back to the presumptive common ancestor of these taxa (Simpson, 1961;Striedter & Northcutt, 1991;Wiley, 1981).…”

Neurophysiological Studies of Learning and Memory in Pigeons

“…It had been known for some time that spatial problems are common following hippocampal lesions in rats (Olton, Becker, & Handelmann, 1979) and humans (Milner, 1965). In some of the early avian studies exploring this issue, Bingman and colleagues had shown that damage to the hippocampus impairs certain aspects of homing in pigeons (Bingman, Ioale, Casini, & Bagnoli, 1990;Bingman & Yates, 1992), and Sherry and Vaccarino (1989) had shown that hippocampal lesions caused disruptions in memory for food caches in black-capped chicka- (Mumby & Pinel, 1994). Thus, what was initially perceived as evidence that the avian hippocampus had a different function to the mammalian hippocampus rapidly became an example of how the avian and mammalian hippocampi shared a similar function: damage to the hippocampus of both species impaired performance on spatial tasks but caused no impairments on visual memory tasks.…”