Evolution of behavioural control in vertebrates

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Amphibian and amniote brains display a conserved general pattern of organization with a few notable differences. The amphibian pattern is much simpler due to a smaller number of larger neurons and less nuclear divisions compared to the situation in mammals and birds. Understanding how this simpler neural substrate functions could provide useful mechanistic information about the core brain pathways controlling behaviour in vertebrates. The long-term goal of my research program is to understand the evolution of neural mechanisms of behavioural control in vertebrates. Our recent work in the fire-bellied toad (Bombina orientalis) showed that behavioural persistence developed with extended training of a prey catching response. Toad prey catching behaviour was at first flexible, but with increased training it became more automatic and persistent, and ultimately, inflexible. Drugs of abuse can also produce persistence by altering behaviour for an exceptionally long period of time, perhaps permanently. However, the specific mechanisms at play are under intense debate. Although sparse, the research done using drugs of abuse in amphibians suggests that these animals could be good models to investigate the basic mechanisms of drug effects on brain and behaviour. Over the next 5 years, I propose to investigate if the behavioural persistence seen in the fire-bellied toad engages multiple aspects of behaviour control and to identify the neural pathways involved in persistence that results from normal learning and drug exposure. The proposed experiments will first investigate the effects of amphetamine exposure on prey catching, a basic motivated behaviour, and then the effects of amphetamine self-administration. Amphetamine is chosen for its ability to enhance behavioural persistence. Emphasis will be on learning paradigms that produce behavioural persistence and control by drug-associated cues. Additionally, reinstatement of extinguished prey catching or drug-seeking responses by drug-associated cues or a drugged state will be investigated to find out if toads display relapse-like behaviour. Finally, investigation of the neural substrate of behavioural persistence and amphetamine effects is planned. The latter will be investigated by measuring the expression of immediate-early genes in the brain, which can be used as an indirect measure of neuronal activity. Throughout the experiments, analyses will assess if a subset of toads are vulnerable to amphetamine effects, thereby mimicking the vulnerability seen in mammals repeatedly exposed to this drug. The findings derived from the proposed work will help to significantly improve our understanding of the basic mechanisms of reward and habit learning in vertebrates, and determine how/if they relate to drug effects. Further, this work could improve our knowledge of how evolutionary innovations in the brain relate to behavioural capacities across vertebrates, something that is poorly understood.