Is bigger always better? A critical appraisal of the use of volumetric analysis in the study of the hippocampus

Abstract

A well-developed spatial memory is important for many animals, but appears especially important for scatter-hoarding species. Consequently, the scatter-hoarding system provides an excellent paradigm in which to study the integrative aspects of memory use within an ecological and evolutionary framework. One of the main tenets of this paradigm is that selection for enhanced spatial memory for cache locations should specialize the brain areas involved in memory. One such brain area is the hippocampus (Hp). Many studies have examined this adaptive specialization hypothesis, typically relating spatial memory to Hp volume. However, it is unclear how the volume of the Hp is related to its function for spatial memory. Thus, the goal of this article is to evaluate volume as a main measurement of the degree of morphological and physiological adaptation of the Hp as it relates to memory. We will briefly review the evidence for the specialization of memory in food-hoarding animals and discuss the philosophy behind volume as the main currency. We will then examine the problems associated with this approach, attempting to understand the advantages and limitations of using volume and discuss alternatives that might yield more specific hypotheses. Overall, there is strong evidence that the Hp is involved in the specialization of spatial memory in scatter-hoarding animals. However, volume may be only a coarse proxy for more relevant and subtle changes in the structure of the brain underlying changes in behaviour. To better understand the nature of this brain/memory relationship, we suggest focusing on more specific and relevant features of the Hp, such as the number or size of neurons, variation in connectivity depending on dendritic and axonal arborization and the number of synapses. These should generate more specific hypotheses derived from a solid theoretical background and should provide a better understanding of both neural mechanisms of memory and their evolution.

Evidence for cache surveillance by a scatter-hoarding rodent

“…Eavesdropping thieves may represent a real cost of cache surveillance in this system. The cache revisiting and inspection behaviours observed in this study are fully consistent with the predictions of the memory enhancement hypothesis (DeGange et al 1989;Brodin 1992;Grubb & Pravosudov 1994;Roth et al 2010), yet they do not conclusively demonstrate that cache surveillance actually serves to strengthen spatial memory. Experimental confirmation is needed to determine whether agouti cache surveillance increases long-term spatial memory and is a mechanism facilitating the ability of agoutis to remember cache locations 120 days after burial.…”

Hummingbirds have a greatly enlarged hippocampal formation

“…Although there are criticisms regarding the combination of data from disparate sources in comparative studies [7,16], it is only by including data for a broader range of species that we could determine with confidence whether hummingbirds have larger HFs than other birds. Furthermore, all of the literature data that we compiled used the same criteria to determine the borders of the HF [15,17].…”

“…To measure volumes of both the HF (electronic supplementary material, figure S1) and the telencephalon, we used the Cavalieri method [11], as implemented in Stereo Investigator (Microbrightfield, Inc., Colchester, VT, USA), because this method is free of measurement bias, is replicable across species and individuals and is frequently used for HF measurements in birds [7,12,13]. We measured the HF and telencephalon on every fourth section of the hummingbird and swift specimens with a 200 mm grid using the same HF borders as earlier studies [14,15].…”

“…Variation in the size of the HF, relative to the telencephalon, in birds often reflects differences in spatial memory; individuals and species with better spatial memory tend to have larger HFs. For example, foodcaching songbirds have relatively larger HFs than songbirds that do not cache food [7,8]. Given this relationship between the relative size of the HF and spatial memory, we predicted that hummingbirds would have HFs that are enlarged in a way similar to that of food-caching parids and corvids.…”

“…Although several studies have investigated the behaviour of hummingbirds with respect to spatialtemporal memories [1 -6], nothing is known about the morphology of the hippocampal formation (HF), which plays a critical role in spatial memory [7,8]. Variation in the size of the HF, relative to the telencephalon, in birds often reflects differences in spatial memory; individuals and species with better spatial memory tend to have larger HFs.…”