Sex, estradiol, and spatial memory in a food-caching corvid

Abstract

Estrogens significantly impact spatial memory function in mammalian species. Songbirds express the estrogen synthetic enzyme aromatase at relatively high levels in the hippocampus and there is evidence from zebra finches that estrogens facilitate performance on spatial learning and/or memory tasks. It is unknown, however, whether estrogens influence hippocampal function in songbirds that naturally exhibit memory-intensive behaviors, such as cache recovery observed in many corvid species. To address this question, we examined the impact of estradiol on spatial memory in non-breeding Western scrub-jays, a species that routinely participates in food caching and retrieval in nature and in captivity. We also asked if there were sex differences in performance or responses to estradiol. Utilizing a combination of an aromatase inhibitor, fadrozole, with estradiol implants, we found that while overall cache recovery rates were unaffected by estradiol, several other indices of spatial memory, including searching efficiency and efficiency to retrieve the first item, were impaired in the presence of estradiol. In addition, males and females differed in some performance measures, although these differences appeared to be a consequence of the nature of the task as neither sex consistently out-performed the other. Overall, our data suggest that a sustained estradiol elevation in a food-caching bird impairs some, but not all, aspects of spatial memory on an innate behavioral task, at times in a sex-specific manner.

Brain estrogen production and the encoding of recent experience

“…In corvids [59] and finches [49], exogenous E2 interferes with hippocampal-dependent spatial memory, which is consistent with recent findings in the prefrontal cortex in aged nonhuman primates [11]. Thus, it may be that the plasticity-enhancing effects of E2 may be deleterious to the faithful initial encoding of a novel sensory stimulus [57].…”

Western scrub-jays do not appear to attend to functionality in Aesop’s Fable experiments

“…Three wild adult male Western scrub-jays ( Aphelocoma californica ) were caught using Potter traps baited with peanuts in southern California (July–August 2013), and one female nestling (BB; an adult at the time of these experiments) was taken from the nest in the summer of 2012 and hand-raised (all captures were authorized under appropriate federal and state collecting permits). Birds were sexed genetically (following Griffiths et al, 1998 ), and the validity of this measure was confirmed via inspection of the gonads by Rensel and colleagues ( 2015 ). Moreover, in Rensel et al (2015) , all four scrub-jays successfully participated in caching experiments, thus indicating their acclimation to captivity.…”

“…Birds were sexed genetically (following Griffiths et al, 1998 ), and the validity of this measure was confirmed via inspection of the gonads by Rensel and colleagues ( 2015 ). Moreover, in Rensel et al (2015) , all four scrub-jays successfully participated in caching experiments, thus indicating their acclimation to captivity. Before and after our experiments, scrub-jays were housed socially with 2–4 birds per aviary (except for BB who was housed singly during a period in which she behaved aggressively toward conspecifics).…”

Data collection in support of the Endocrine Disruption (ED) assessment for non‐target vertebrates

“…The method for improving sex-steroid extraction from plasma for RIA detailed in Newman et al (2008) has been used (cited) by researchers working primarily with bird tissues (e.g. Taves et al 2010, Shah et al 2011, Fokidis et al 2013Dickens et al 2014, Heimovics et al 2016, Prior et al 2017, Merrill et al 2019, although it has also been employed with lizard (Zena et al 2019), snakes (Rensel et al 2015), fish (Lorenzi et al 2012) and mouse (Overk et al 2013) samples. There was also some cross-over with many of the papers which cited the SPE extraction methods of Newman et al also citing Charlier et al (2010) SPE method for extracting steroids from tissues (brain) for RIA or Chao et al (2011) liquid-liquid plus SPE method for plasma and tissues extraction for ELISA.…”