Abstract
Filial imprinting of domestic chicks has a well-defined sensitive (critical) period lasting in the laboratory from hatching to day 3. It is a typical model to investigate the molecular mechanisms underlying memory formation in early learning. We recently found that thyroid hormone 3,5,3′-triiodothyronine (T3) is a determinant of the sensitive period. Rapid increases in cerebral T3 levels are induced by imprinting training, rendering chicks imprintable. Furthermore, the administration of exogenous T3 makes chicks imprintable on days 4 or 6 even after the sensitive period has ended. However, how T3 affects neural transmission to enable imprinting remains mostly unknown. In this study, we demonstrate opposing roles for gamma-aminobutyric acid (GABA)-A and GABA-B receptors in imprinting downstream of T3. Quantitative reverse transcription polymerase chain reaction and immunoblotting showed that the GABA-A receptor expression increases gradually from days 1 to 5, whereas the GABA-B receptor expression gradually decreases. We examined whether neurons in the intermediate medial mesopallium (IMM), the brain region responsible for imprinting, express both types of GABA receptors. Immunostaining showed that morphologically identified putative projection neurons express both GABA-A and GABA-B receptors, suggesting that those GABA receptors interact with each other in these cells to modulate the IMM outputs. The roles of GABA-A and GABA-B receptors were investigated using various agonists and antagonists. Our results show that GABA-B receptor antagonists suppressed imprinting on day 1, while its agonists made day 4 chicks imprintable without administration of exogenous T3. By contrast, GABA-A receptor agonists suppressed imprinting on day 1, while its antagonists induced imprintability on day 4 without exogenous T3. Furthermore, both GABA-A receptor agonists and GABA-B receptor antagonists suppressed T3-induced imprintability on day 4 after the sensitive period has ended. Our data from these pharmacological experiments indicate that GABA-B receptors facilitate imprinting downstream of T3 by initiating the sensitive period, while the GABA-A receptor contributes to the termination of the sensitive period. In conclusion, we propose that opposing roles of GABA-A and GABA-B receptors in the brain during development determine the induction and termination of the sensitive period.
Highlights
Hatched chicks undergo filial imprinting, a process in which they memorize and follow their mother in order to receive care (Lorenz, 1937; Vallortigara and Versace, 2018)
Pena and colleagues recently showed that T3 activates the mechanistic target of rapamycin, which has been implicated in long-term potentiation (LTP) and long-term memory, in the intermediate medial mesopallium (IMM) neurons and that mTOR activation by an Akt activator made day 4 chicks imprintable similar to the described T3 effects (Batista et al, 2018)
The preference scores of chicks injected with the gamma-aminobutyric acid (GABA)-A receptor agonist muscimol were not significantly different from those of control chicks (Figure 2F). These results demonstrate that a reduction in GABA-A receptor signaling made day 4 chicks imprintable without administration of T3 and that GABA-A receptor signaling was downstream of T3
Summary
Hatched chicks undergo filial imprinting, a process in which they memorize and follow their mother in order to receive care (Lorenz, 1937; Vallortigara and Versace, 2018). Imprinting has clearly a sensitive or critical period after which chicks cannot be imprinted (Hess, 1959). The molecular mechanisms of memory formation in imprinting have been investigated intensively (Horn, 2004; Yamaguchi et al, 2008a,b, 2010, 2011; Solomonia and McCabe, 2015). Intravenous T3 injection into the intermediate medial mesopallium (IMM), a critical brain area for imprinting acquisition (McCabe et al, 1981), makes chicks imprintable even after the sensitive period has closed. Chicks injected with T3 on day 1 can be imprinted on days 4–8. The exogenous injection of transmitters or hormones, e.g., norepinephrine, serotonin, dopamine, and testosterone, did not influence the imprintability of chicks, suggesting that they cannot be substituted for T3 (Yamaguchi et al, 2012)
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