Assignment of model amygdala neurons to the fear memory trace depends on competitive synaptic interactions - PubMed (original) (raw)
Assignment of model amygdala neurons to the fear memory trace depends on competitive synaptic interactions
Dongbeom Kim et al. J Neurosci. 2013.
Abstract
We used biophysical modeling to examine a fundamental, yet unresolved, question regarding how particular lateral amygdala (LA) neurons are assigned to fear memory traces. This revealed that neurons with high intrinsic excitability are more likely to be integrated into the memory trace, but that competitive synaptic interactions also play a critical role. Indeed, when the ratio of intrinsically excitable cells was increased or decreased, the number of plastic cells remained relatively constant. Analysis of the connectivity of plastic and nonplastic cells revealed that subsets of principal LA neurons effectively band together by virtue of their excitatory interconnections to suppress plasticity in other principal cells via the recruitment of inhibitory interneurons.
Figures
Figure 1.
Spatial structure, intrinsic connectivity, and fear-conditioning protocol for the LAd network model. A, The model consists of 800 principal cells and 200 interneurons populated randomly in the horn-shaped LAd. B, Fear-conditioning protocol. C, Average tone responses of plastic LAd cells during the different phases of the behavioral protocol. D, Example of tone responses generated by a plastic cell during habituation (top) and recall test (bottom). E, Repetitive firing dynamics of three types of model projection cells. F, Proportion of plastic cells among the three types of projection cells. G, Expected (white) and observed (black) numbers of model plastic cells for the control, CREB+, and CREB− cases. Competition biases the observed numbers toward the control value.
Figure 2.
Differential intrinsic connectivity supports competition. A–F, Monosynaptic excitatory (A, C, E) and disynaptic inhibitory (B, D, F) connections among as well as between plastic and nonplastic cells (_x_-axis) in the control case. C–F, Connections of type B or C winner and loser cells in the CREB+ (C, D) and CREB− (E, F) simulations. A and B consider connections between all plastic and nonplastic principal cells. In contrast, C–F consider connections between the subsets of plastic or nonplastic cells only, and so the numbers are smaller. Data are averages ± SEM.
Similar articles
- Synaptic competition in the lateral amygdala and the stimulus specificity of conditioned fear: a biophysical modeling study.
Kim D, Samarth P, Feng F, Pare D, Nair SS. Kim D, et al. Brain Struct Funct. 2016 May;221(4):2163-82. doi: 10.1007/s00429-015-1037-4. Epub 2015 Apr 10. Brain Struct Funct. 2016. PMID: 25859631 Free PMC article. - Mechanisms underlying the formation of the amygdalar fear memory trace: A computational perspective.
Feng F, Samarth P, Paré D, Nair SS. Feng F, et al. Neuroscience. 2016 May 13;322:370-6. doi: 10.1016/j.neuroscience.2016.02.059. Epub 2016 Mar 2. Neuroscience. 2016. PMID: 26944604 Free PMC article. - Synaptic plasticity associated with a memory engram in the basolateral amygdala.
Nonaka A, Toyoda T, Miura Y, Hitora-Imamura N, Naka M, Eguchi M, Yamaguchi S, Ikegaya Y, Matsuki N, Nomura H. Nonaka A, et al. J Neurosci. 2014 Jul 9;34(28):9305-9. doi: 10.1523/JNEUROSCI.4233-13.2014. J Neurosci. 2014. PMID: 25009263 Free PMC article. - Synaptic transmission and plasticity in the amygdala. An emerging physiology of fear conditioning circuits.
Maren S. Maren S. Mol Neurobiol. 1996 Aug;13(1):1-22. doi: 10.1007/BF02740749. Mol Neurobiol. 1996. PMID: 8892333 Review. - Genes and mechanisms in the amygdala involved in the formation of fear memory.
Pape HC, Stork O. Pape HC, et al. Ann N Y Acad Sci. 2003 Apr;985:92-105. doi: 10.1111/j.1749-6632.2003.tb07074.x. Ann N Y Acad Sci. 2003. PMID: 12724151 Review.
Cited by
- The Role of Intrinsic Plasticity in Engram Physiology and Temporal Memory Linking.
Peregrim W, O'Leary T. Peregrim W, et al. J Neurosci. 2024 Sep 11;44(37):e1160242024. doi: 10.1523/JNEUROSCI.1160-24.2024. J Neurosci. 2024. PMID: 39261012 Review. No abstract available. - Inhibitory circuits in fear memory and fear-related disorders.
Singh S, Topolnik L. Singh S, et al. Front Neural Circuits. 2023 Mar 23;17:1122314. doi: 10.3389/fncir.2023.1122314. eCollection 2023. Front Neural Circuits. 2023. PMID: 37035504 Free PMC article. Review. - The Interplay of Synaptic Plasticity and Scaling Enables Self-Organized Formation and Allocation of Multiple Memory Representations.
Auth JM, Nachstedt T, Tetzlaff C. Auth JM, et al. Front Neural Circuits. 2020 Oct 7;14:541728. doi: 10.3389/fncir.2020.541728. eCollection 2020. Front Neural Circuits. 2020. PMID: 33117130 Free PMC article. - Neurophotonics Approaches for the Study of Pattern Separation.
Morales C, Morici JF, Miranda M, Gallo FT, Bekinschtein P, Weisstaub NV. Morales C, et al. Front Neural Circuits. 2020 Jun 9;14:26. doi: 10.3389/fncir.2020.00026. eCollection 2020. Front Neural Circuits. 2020. PMID: 32587504 Free PMC article. Review. - The role of intrinsic excitability in the evolution of memory: Significance in memory allocation, consolidation, and updating.
Chen L, Cummings KA, Mau W, Zaki Y, Dong Z, Rabinowitz S, Clem RL, Shuman T, Cai DJ. Chen L, et al. Neurobiol Learn Mem. 2020 Sep;173:107266. doi: 10.1016/j.nlm.2020.107266. Epub 2020 Jun 5. Neurobiol Learn Mem. 2020. PMID: 32512183 Free PMC article. Review.
References
- Carnevale NT, Hines ML. The NEURON book. Cambridge, UK: Cambridge UP; 2006.
- Faber ES, Callister RJ, Sah P. Morphological and electrophysiological properties of principal neurons in the rat lateral amygdala in vitro. J Neurophysiol. 2001;85:714–723. - PubMed
Publication types
MeSH terms
LinkOut - more resources
Full Text Sources
Other Literature Sources
Medical