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The Journal of Neuroscience, April 13, 2005, 25(15):3881-3888; doi:10.1523/JNEUROSCI.0416-05.2005

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Behavioral/Systems/Cognitive
Role of Amygdalo-Nigral Circuitry in Conditioning of a Visual Stimulus Paired with Food

Hongjoo J. Lee, Frank Groshek, Gorica D. Petrovich, Joseph P. Cantalini, Michela Gallagher, and Peter C. Holland

Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, Maryland 21218

The amygdala central nucleus (CeA) plays an important part in associative learning. Although most research has focused on functions of its descending projections to brainstem areas involved in autonomic and somatomotor responses, the ascending projections of CeA also play critical roles in learning. For example, a CeA-nigrostriatal pathway is important for acquiring orienting responses (ORs) to conditioned stimuli (CSs) that signal food delivery. In this study, the function of this CeA-nigrostriatal pathway in appetitive conditioning of rats was considered in more detail.

In experiment 1, we combined anatomical tracing and methods for detecting neuronal activation to examine whether CeA neurons that project to the substantia nigra pars compacta (SNc) are activated by a visual CS for food. After injection of the retrograde tracer Fluoro-Gold (FG) into SNc, the rats received pairings of a visual CS with food. After a test with the CS alone, the brains were prepared to assess FG labeling and CS-induced Fos expression in CeA with immunohistochemical procedures. Colocalization of Fos and FG in CeA neurons was visualized with confocal-fluorescence microscopy. The CS induced Fos expression in CeA, and a majority of these Fos-positive neurons were also FG positive, indicating activation of the CeA-SNc pathway by the CS. In experiment 2, lesions that disconnected CeA and SNc prevented the acquisition of conditioned ORs but did not affect the acquisition of conditioned food-related responses or the display of unconditioned ORs. These experiments demonstrate a role for amygdalo-nigral circuitry in learned modulation of attention to signals for biologically significant events.

Key words: amygdala; central nucleus; substantia nigra; appetitive conditioning; retrograde labeling; Fos activation; dorsolateral striatum

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Received Dec 8, 2004; revised March 1, 2005; accepted March 6, 2005.

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