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Dopamine-mediated modulation of odour-evoked amygdala potentials during pavlovian conditioning

Abstract

Pavlovian conditioning results when an innocuous stimulus, such as an odour, is paired with a behaviourally relevant stimulus, such as a foot-shock, so that eventually the former stimulus alone will elicit the behavioural response of the latter. The lateral nucleus of the amygdala (LAT) is necessary for the emotional memory formation in this paradigm1,2,3,4. Enhanced neuronal firing in LAT to conditioned stimuli emerge in parallel with the behavioural changes5,6,7,8,9,10,11 and are dependent on local dopamine12,13,14,15. To study the changes in neuronal excitability and synaptic drive that contribute to the pavlovian conditioning process, here we used in vivo intracellular recordings to examine LAT neurons during pavlovian conditioning in rats. We found that repeated pairings of an odour with a foot-shock resulted in enhanced post-synaptic potential (PSP) responses to the odour and increased neuronal excitability. However, a non-paired odour displayed PSP decrement. The dopamine antagonist haloperidol blocked the PSP enhancement and associated increased neuronal excitability, without reversing previous conditioning. These results demonstrate that conditioning and habituation processes produce opposite effects on LAT neurons and that dopamine is important in these events, consistent with its role in emotional memory formation.

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Figure 1: Stimulus-evoked responses in amygdala (LAT) neurons.
Figure 2: Opposing effects of habituation and conditioning on LAT neurons.
Figure 3: Dopamine receptor antagonism blocks enhancement of the odour-evoked response caused by the conditioning procedure.
Figure 4: Neuronal excitability is enhanced by the conditioning procedure, which is blocked by dopamine receptor antagonism.
Figure 5: The pavlovian conditioning procedure reduces spontaneous PSPs via dopamine receptor activation.

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Acknowledgements

We thank N. MacMurdo, C. Smolak and B. Lowry for technical assistance, and H. Moore, A. R. West and S. Stocker for discussions. Support was provided by National Institutes of Health grants.

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Correspondence to J. Amiel Rosenkranz.

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Rosenkranz, J., Grace, A. Dopamine-mediated modulation of odour-evoked amygdala potentials during pavlovian conditioning. Nature 417, 282–287 (2002). https://doi.org/10.1038/417282a

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