The impact of brain development, context change, individual differences, and entropy on animal habituation

In a world full of information, animals have evolved cognitive mechanisms to ignore irrelevant stimuli and selectively focus on important ones. Among these mechanisms, those controlling habituation allow the suppression of the response elicited by irrelevant stimuli that repeat over time. To better understand this behavioral and phenomenon, we capitalized on the domestic chick (Gallus gallus), whose brain develops almost completely in the egg, which makes this animal mobile and independent from parental cares soon after hatching. By testing chicks from the first day after hatching we found that the neural mechanisms underlying habituation are immediately active in chicks, but newborn chicks can habituate to a greater extent than older animals. This shows an early period of increased plasticity in the chick brain that rapidly decreases in the first three days after hatching. Together with habituation, we found that dishabituation is also fully developed in newborn chicks. Comparator theories of habituation predict that both mechanisms stem from a common memory mechanism. Our results represent the first evidence to support this conclusion using a developmental approach. Previous studies have shown that habituation is context-specific and cannot be entirely transferred to a new context. We reviewed the evidence in support of this conclusion and demonstrated that the neural mechanisms underlying context-specific habituation are functional in chicks’ embryos and modulate the postnatal recalling of a habituated response acquired prenatally. We found context-specific habituation also in an invertebrate species phylogenetically distant from the domestic chick, the bumblebee (Bombus terrestris). This result adds to the existing evidence that the cognitive mechanisms underlying context-specific habituation are widespread in the animal reign, irrespective of the complexity of the nervous systems considered. Before exploring context-specific habituation in bumblebees, we developed a new paradigm to study habituation and dishabituation of the defensive behaviour in this species. By testing several behavioural traits of inexperienced chicks and measuring their body size, we found that more exploratory chicks have greater variability of habituation rate than less exploratory ones. This variability is linked to the body size of the more exploratory chicks. Bigger chicks are more responsive to a loud sound but habituate to a greater extent than smaller ones. Since in our experiments chicks were born and reared in a controlled environment, our results suggest that an innate biological factor may be involved in the covariation between exploration, body size and habituation. We studied the generalization capacity of the invasive crayfish Procambarus clarkii. By using a habituation-dishabituation paradigm we found that crayfish can transfer a habituated response to a new stimulus. Generalization takes place after a single trial in which the new stimulus is presented following the habituation one and last for at least 45 days. Generalization may contribute to the superior behavioural flexibility of this invasive crayfish compared to native species. Finally, together we developed a new model of rate-sensitivity of habituation. This model accounts for the information conveyed by the temporal sequence of stimulus repetitions exploiting the notion of entropy. We found that the amount of habituation of the freezing response elicited by a loud sound decreases as a function of the entropy apported by a new stimulus repetition. Overall, our findings support comparator theories of habituation and provide strong evidence in support of the associative nature of habituation.