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The structure of Pavlovian fear conditioning in the amygdala

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Abstract

Do different brains forming a specific memory allocate the same groups of neurons to encode it? One way to test this question is to map neurons encoding the same memory and quantitatively compare their locations across individual brains. In a previous study, we used this strategy to uncover a common topography of neurons in the dorsolateral amygdala (LAd) that expressed a learning-induced and plasticity-related kinase (p42/44 mitogen-activated protein kinase; pMAPK), following auditory Pavlovian fear conditioning. In this series of experiments, we extend our initial findings to ask to what extent this functional topography depends upon intrinsic neuronal structure. We first showed that the majority (87 %) of pMAPK expression in the lateral amygdala was restricted to principal-type neurons. Next, we verified a neuroanatomical reference point for amygdala alignment using in vivo magnetic resonance imaging and in vitro morphometrics. We then determined that the topography of neurons encoding auditory fear conditioning was not exclusively governed by principal neuron cytoarchitecture. These data suggest that functional patterning of neurons undergoing plasticity in the amygdala following Pavlovian fear conditioning is specific to memory formation itself. Further, the spatial allocation of activated neurons in the LAd was specific to cued (auditory), but not contextual, fear conditioning. Spatial analyses conducted at another coronal plane revealed another spatial map unique to fear conditioning, providing additional evidence that the functional topography of fear memory storing cells in the LAd is non-random and stable. Overall, these data provide evidence for a spatial organizing principle governing the functional allocation of fear memory in the amygdala.

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Acknowledgments

We are very grateful to Dr Robert Ursano and the Center for the Study of Traumatic Stress (CSTS) for support. We thank Dr Alex McDonald for advice on the CaMKII antibody and Dr Jennifer McGuire for advice on immunofluorescence. Supported by Grants USU #NW188NW and USU #NWI88NZ.

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Authors and Affiliations

  1. Department of Psychiatry, School of Medicine, Uniformed Services University (USU), Bethesda, MD, 20814, USA

    Hadley C. Bergstrom & Luke R. Johnson

  2. Program in Neuroscience, School of Medicine, Uniformed Services University (USU), Bethesda, MD, 20814, USA

    Luke R. Johnson

  3. Center for the Study of Traumatic Stress (CSTS), School of Medicine, Uniformed Services University (USU), Bethesda, MD, 20814, USA

    Luke R. Johnson

  4. Center for Neuroscience and Regenerative Medicine (CNRM), School of Medicine, Uniformed Services University (USU), Bethesda, MD, 20814, USA

    Smita Dey, Haying Tang, Reed G. Selwyn & Luke R. Johnson

  5. Department of Radiology, Uniformed Services University (USU), School of Medicine, Bethesda, MD, USA

    Haying Tang & Reed G. Selwyn

  6. Department of Psychology, George Mason University, Fairfax, VA, USA

    Craig G. McDonald

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  1. Hadley C. Bergstrom
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  2. Craig G. McDonald
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  3. Smita Dey
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  4. Haying Tang
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  6. Luke R. Johnson
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Correspondence to Luke R. Johnson.

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Bergstrom, H.C., McDonald, C.G., Dey, S. et al. The structure of Pavlovian fear conditioning in the amygdala. Brain Struct Funct 218, 1569–1589 (2013). https://doi.org/10.1007/s00429-012-0478-2

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  • DOI: https://doi.org/10.1007/s00429-012-0478-2

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