Variation in memory and the hippocampus across populations from different climates: a common garden approach

Abstract

Selection for enhanced cognitive traits is hypothesized to produce enhancements to brain structures that support those traits. Although numerous studies suggest that this pattern is robust, there are several mechanisms that may produce this association. First, cognitive traits and their neural underpinnings may be fixed as a result of differential selection on cognitive function within specific environments. Second, these relationships may be the product of the selection for plasticity, where differences are produced owing to an individual's experiences in the environment. Alternatively, the relationship may be a complex function of experience, genetics and/or epigenetic effects. Using a well-studied model species (black-capped chickadee, Poecile atricapillus), we have for the first time, to our knowledge, addressed these hypotheses. We found that differences in hippocampal (Hp) neuron number, neurogenesis and spatial memory previously observed in wild chickadees persisted in hand-raised birds from the same populations, even when birds were raised in an identical environment. These findings reject the hypothesis that variation in these traits is owing solely to differences in memory-based experiences in different environments. Moreover, neuron number and neurogenesis were strikingly similar between captiveraised and wild birds from the same populations, further supporting the genetic hypothesis. Hp volume, however, did not differ between the captive-raised populations, yet was very different in their wild counterparts, supporting the experience hypothesis. Our results indicate that the production of some Hp factors may be inherited and largely independent of environmental experiences in adult life, regardless of their magnitude, in animals under high selection pressure for memory, while traits such as volume may be more plastic and modified by the environment.

Hummingbirds have a greatly enlarged hippocampal formation

“…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].…”

Pharmacological evidence is consistent with a prominent role of spatial memory in complex navigation

“…Many studies demonstrate that species with behaviours that might rely on spatial memory (e.g. migration) tend to have enhanced spatial memory performance in the laboratory [3,17,18]. Although informative in many respects, this approach provides only correlative evidence of a relationship between cognition and navigation (sensu [19,20]).…”

Seasonal variation in corticosterone receptor binding in brain, hippocampus, and gonads in House Sparrows (Passer domesticus)

“…Although brain shows a highly heterogeneous distribution of GR and MR (Morimoto et al 1996), we used a whole-brain assay to be able to compare the results to previous work (Breuner and Orchinik 2001). We also examined CORT receptor binding in the hippocampus, an area involved in CORT negative feedback regulation in mammals (Jacobson andSapolsky 1991, Jacobson 2005) and in CORT-sensitive memory formation and storage in birds (Pravosudov 2003(Pravosudov , 2005Roth et al 2012). House Sparrows show seasonal patterns in CORT concentrations similar to those in many other seasonally breeding vertebrates (Romero et al 2006, Lattin et al 2012a; furthermore, because their CORT receptors have been fully characterized in both brain (Breuner and Orchinik 2009) and gonads (Lattin et al 2012b), they are an excellent subject for this type of study.…”