The Rostral Anterior Cingulate Cortex Modulates the Efficiency of Amygdala-Dependent Fear Learning

Stephanie Bissiere, Nicolas Daniel Plachta, Daniel Hoyer, Kevin H McAllister, Hans-Rudolf Olpe, Anthony A Grace, John F Cryan

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Abstract

Background: The rostral anterior cingulate cortex (rACC) and the amygdala consistently emerge from neuroimaging studies as brain regions crucially involved in normal and abnormal fear processing. To date, however, the role of the rACC specifically during the acquisition of auditory fear conditioning still remains unknown. The aim of this study is to investigate a possible top-down control of a specific rACC sub-region over amygdala activation during pavlovian fear acquisition. Methods: We performed excitotoxic lesions, temporal inactivation, and activation of a specific sub-region of the rACC that we identified by tracing studies as supporting most of the connectivity with the basolateral amygdala (rAmy-ACC). The effects of these manipulations over amygdala function were investigated with a classical tone-shock associative fear conditioning paradigm in the rat. Results: Excitotoxic lesions and transient inactivation of the rAmy-ACC pre-training selectively produced deficits in the acquisition of the tone-shock associative learning (but not context). This effect was specific for the acquisition phase. However, the deficit was found to be transient and could be overcome by overtraining. Conversely, pre-training transient activation of the rAmy-ACC facilitated associative learning and increased fear expression. Conclusions: Our results suggest that a subregion of the rACC is key to gating the efficiency of amygdala-dependent auditory fear conditioning learning. Because rAmy-ACC inputs were confirmed to be glutamatergic, we propose that recruitment of this brain area might modulate overall basolateral amygdala excitatory tone during conditioned stimulus-unconditioned stimulus concomitant processing. In the light of clinical research, our results provide new insight on the effect of inappropriate rACC recruitment during emotional events.
Original languageEnglish
Pages (from-to)821 - 831
Number of pages11
JournalBiological Psychiatry
Volume63
Issue number9
DOIs
Publication statusPublished - 2008
Externally publishedYes

Cite this

Bissiere, S., Plachta, N. D., Hoyer, D., McAllister, K. H., Olpe, H-R., Grace, A. A., & Cryan, J. F. (2008). The Rostral Anterior Cingulate Cortex Modulates the Efficiency of Amygdala-Dependent Fear Learning. Biological Psychiatry, 63(9), 821 - 831. https://doi.org/10.1016/j.biopsych.2007.10.022