Context-specific effects of estradiol on spatial learning and memory in the zebra finch

Abstract

Estradiol is known to impact cognitive function including spatial learning and memory, with studies focused largely on rodent models. Estrogens can be produced peripherally or centrally as neuroestrogens, and the specific role for neuroestrogens in memory processes remains unresolved. Many songbirds possess remarkable spatial memory capabilities and also express the estrogen synthetic enzyme aromatase abundantly in the hippocampus, suggesting that locally-produced estrogens may promote the acquisition or retrieval of spatial memories in these birds. We examined the effect of estradiol on spatial memory in three contexts in the zebra finch: retrieval after discrimination training, retrieval after familiarization but without discrimination training, and memory acquisition, using a combination of estradiol implants and oral dosing with the aromatase inhibitor fadrozole (FAD). Retrieval of spatial memory in both contexts was impaired when estradiol production was blocked. However, spatial memory acquisition was enhanced when estradiol production was inhibited whereas estradiol replacement impaired acquisition. These results provide evidence for a context-specific role of estradiol in songbird spatial memory, results that finds accord with some mammalian studies but have not yet been observed in birds.

Across sex and age: Learning and memory and patterns of avian hippocampal gene expression.

“…These results are also in line with observations in other regions of the songbird brain where IEG expression is elevated in females (Krentzel & Remage-Healey, 2015). Such a sex-difference could result from differences in actions of estrogens, which have been shown to alter behavior on a similar HP-dependent spatial memory task (Rensel et al, 2013), potentially by altering the balance of HP excitability. Alternatively, and as discussed above, it may be that females employ somewhat different strategies to solve the task (Kanit et al, 2000; Tropp & Markus, 2001), engaging the HP to a greater degree resulting in increased Egr-1 expression, or perhaps in order to compensate for a tendency towards deficient spatial processing.…”

“…To explore the effects of age and sex on spatial memory function in a songbird, we adapted a previously used task that involves acquisition and recall of a food reward in a 4-arm maze (Rensel, Salwiczek, Roth, & Schlinger, 2013). This particular task demands that animals use place-learning strategies involving allocentric cues to locate a reward.…”

The importance of neural aromatization in the acquisition, recall, and integration of song and spatial memories in passerines

“…Combinations of E 2 implants and inhibition of aromatase synthesis with fadrozole in zebra finches suggests more of a role for E 2 in the retrieval rather than the acquisition of a location in a four-arm maze (Rensel et al, 2013). Oberlander et al (2004) castrated adult male zebra finches and implanted them subcutaneously with blanks, testosterone, dihydrotestosterone (DHT), or E 2 .…”

“…Also, levels of E 2 in brain were much higher than those in plasma, suggesting that the primarily synaptic aromatization in the hippocampus is crucial to . Moreover, while modulation of local or global E 2 production affects spatial memory in zebra finches (Oberlander et al, 2004;Bailey et al, 2013;Rensel et al, 2013), what remains unclear is whether failures of retrieval in these various tests are due to inabilities of hippocampal cells to acquire, consolidate, retain, or recall the spatial tasks. Measurement or more temporallyspecific manipulation of locally-produced E 2 during acquisition and retention phases may more precisely specify the role of neural aromatization.…”

Steroids in the avian brain: heterogeneity across space and time

“…Two examples help illustrate these points. First, there is evidence that estrogens act on the hippocampus (HP) to influence a bird's ability to find food and remember where available food exists in a maze or in an open arena (Bailey et al 2013; Oberlander et al 2004; Rensel et al 2013). The estrogen synthetic enzyme aromatase is expressed in relatively high amounts in the songbird HP where it remains elevated, or even increases, outside of the breeding season (Saldanha et al 1999; Saldanha et al 1998; Soma 1999.…”