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New Research, Sensory and Motor Systems

Intrinsic Circuits in the Lateral Central Amygdala

Sarah Hunt, Yajie Sun, Hakan Kucukdereli, Rüdiger Klein and Pankaj Sah
eNeuro 23 February 2017, ENEURO.0367-16.2017; https://doi.org/10.1523/ENEURO.0367-16.2017
Sarah Hunt
1Queensland Brain Institute, The University of Queensland, Brisbane, Queensland 4072, Australia
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Yajie Sun
1Queensland Brain Institute, The University of Queensland, Brisbane, Queensland 4072, Australia
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Hakan Kucukdereli
2Max Planck Institute of Neurobiology, Am Klopferspitz 18, Martinsreid 82152, Germany
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Rüdiger Klein
2Max Planck Institute of Neurobiology, Am Klopferspitz 18, Martinsreid 82152, Germany
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Pankaj Sah
1Queensland Brain Institute, The University of Queensland, Brisbane, Queensland 4072, Australia
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Abstract

Network activity in the lateral central amygdala (CeL) plays a crucial role in fear learning and emotional processing. However, the local circuits of the CeL are not fully understood and have only recently begun to be explored in detail. Here, we characterised the intrinsic circuits in the CeL using paired whole-call patch-clamp recordings, immunohistochemistry and optogenetics in C57/BLJ6 wildtype and somatostatin-cre (SOM-Cre) mice. Our results revealed that throughout the rostro-caudal extent of the CeL, neurons form inhibitory connections at a rate of ∼29% with an average amplitude of 20 ± 3 pA (at -40 mV). Inhibitory input from a single neuron is sufficient to halt firing in the postsynaptic neuron. Post-hoc immunostaining for protein kinase C δ (PKCδ) in wildtype mice and paired recordings in SOM-Cre mice demonstrated that the most common local connections were PKCδ(-)→PKCδ(-), and SOM(+)→SOM(+). Finally, by optogenetically activating either SOM(+) or SOM(-) neurons, we found that almost all neurons in the CeL were innervated by these neuronal populations, and that connections between like-neurons were stronger than those between different neuronal types. These findings reveal a complex network of connection within the CeL, and provide the foundations for future behaviour-specific circuit analysis of this complex network.

Significance Local inhibition in the lateral central amygdala (CeL) plays a crucial role in the processing of emotions, yet a complete understanding of these connections is still in its infancy. In this study, we show that CeL neurons are highly interconnected and that inhibition from a single neuron is sufficient to silence the postsynaptic neuron. Focusing on two well-known CeL neuronal subtypes: protein kinase C δ (PKCδ)- and somatostatin (SOM)-expressing neurons, we show that the most common local connections are PKCδ(-)→PKCδ(-) and SOM(+)→SOM(+). Optogenetic activation of either SOM(+) or SOM(-) neuronal populations revealed that inhibition was larger between like-neurons. These findings show that within the CeL there is a complex network, and provide the foundations for future behavior-specific circuit studies.

  • anxiety
  • emotion
  • fear
  • learning

Footnotes

  • Authors report no conflict of interest.

  • This work was supported by grants to PS from the National Health and Medical Research Council and the Australian Research Council. The authors declare no financial or non-financial competing interests.

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Intrinsic Circuits in the Lateral Central Amygdala
Sarah Hunt, Yajie Sun, Hakan Kucukdereli, Rüdiger Klein, Pankaj Sah
eNeuro 23 February 2017, ENEURO.0367-16.2017; DOI: 10.1523/ENEURO.0367-16.2017

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Intrinsic Circuits in the Lateral Central Amygdala
Sarah Hunt, Yajie Sun, Hakan Kucukdereli, Rüdiger Klein, Pankaj Sah
eNeuro 23 February 2017, ENEURO.0367-16.2017; DOI: 10.1523/ENEURO.0367-16.2017
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