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The Journal of Neuroscience, June 29, 2005, 25(26):6066-6075; doi:10.1523/JNEUROSCI.1168-05.2005

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Behavioral/Systems/Cognitive
A Subpopulation of Neurons in the Medial Prefrontal Cortex Encodes Emotional Learning with Burst and Frequency Codes through a Dopamine D₄ Receptor-Dependent Basolateral Amygdala Input

Steven R. Laviolette,¹ Witold J. Lipski,¹ and Anthony A. Grace^1,2,3

Departments of ¹Neuroscience, ²Psychiatry, and ³Psychology, University of Pittsburgh, Pittsburgh, Pennsylvania 15260

The basolateral nucleus of the amygdala (BLA) and medial prefrontal cortex (mPFC) are involved importantly in the processing and encoding of emotionally salient learned associations. Here, we examined the possible role of the mPFC in the acquisition and encoding of emotional associative learning at the behavioral and single-neuron level. A subpopulation of neurons in the mPFC that received monosynaptic and orthodromic inputs from the BLA demonstrated strong associative responding to odors paired previously with footshock by increasing spontaneous activity and bursting activity. This occurred specifically in response to postconditioning presentations of the footshock-paired odors but not to odors presented in the absence of footshock. In contrast, mPFC neurons that failed to respond to BLA stimulation showed no associative responding. Systemic or intra-mPFC blockade of dopamine (DA) D₄ receptors prevented this emotional associative learning in neurons of the mPFC and blocked the expression of olfactory conditioned fear. These results demonstrate that individual neurons in the mPFC that receive a functional input from the BLA actively encode emotional learning and that this process depends on DA D₄ receptor stimulation in the mPFC.

Key words: amygdala; cortex; learning; neuron; plasticity; dopamine receptor; prefrontal cortex

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Received March 24, 2005; revised May 6, 2005; accepted May 14, 2005.

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