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Inhibitory Gating of Basolateral Amygdala Inputs to the Prefrontal Cortex.
J Neurosci 2016; 36(36):9391-406JN

Abstract

Interactions between the prefrontal cortex (PFC) and basolateral amygdala (BLA) regulate emotional behaviors. However, a circuit-level understanding of functional connections between these brain regions remains incomplete. The BLA sends prominent glutamatergic projections to the PFC, but the overall influence of these inputs is predominantly inhibitory. Here we combine targeted recordings and optogenetics to examine the synaptic underpinnings of this inhibition in the mouse infralimbic PFC. We find that BLA inputs preferentially target layer 2 corticoamygdala over neighboring corticostriatal neurons. However, these inputs make even stronger connections onto neighboring parvalbumin and somatostatin expressing interneurons. Inhibitory connections from these two populations of interneurons are also much stronger onto corticoamygdala neurons. Consequently, BLA inputs are able to drive robust feedforward inhibition via two parallel interneuron pathways. Moreover, the contributions of these interneurons shift during repetitive activity, due to differences in short-term synaptic dynamics. Thus, parvalbumin interneurons are activated at the start of stimulus trains, whereas somatostatin interneuron activation builds during these trains. Together, these results reveal how the BLA impacts the PFC through a complex interplay of direct excitation and feedforward inhibition. They also highlight the roles of targeted connections onto multiple projection neurons and interneurons in this cortical circuit. Our findings provide a mechanistic understanding for how the BLA can influence the PFC circuit, with important implications for how this circuit participates in the regulation of emotion.

SIGNIFICANCE STATEMENT

The prefrontal cortex (PFC) and basolateral amygdala (BLA) interact to control emotional behaviors. Here we show that BLA inputs elicit direct excitation and feedforward inhibition of layer 2 projection neurons in infralimbic PFC. BLA inputs are much stronger at corticoamygdala neurons compared with nearby corticostriatal neurons. However, these inputs are even more powerful at parvalbumin and somatostatin expressing interneurons. BLA inputs thus activate two parallel inhibitory networks, whose contributions change during repetitive activity. Finally, connections from these interneurons are also more powerful at corticoamygdala neurons compared with corticostriatal neurons. Together, our results demonstrate how the BLA predominantly inhibits the PFC via a complex sequence involving multiple cell-type and input-specific connections.

Authors+Show Affiliations

Center for Neural Science, New York University, New York, New York 10003.Center for Neural Science, New York University, New York, New York 10003 adam.carter@nyu.edu.

Pub Type(s)

Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

27605614

Citation

McGarry, Laura M., and Adam G. Carter. "Inhibitory Gating of Basolateral Amygdala Inputs to the Prefrontal Cortex." The Journal of Neuroscience : the Official Journal of the Society for Neuroscience, vol. 36, no. 36, 2016, pp. 9391-406.
McGarry LM, Carter AG. Inhibitory Gating of Basolateral Amygdala Inputs to the Prefrontal Cortex. J Neurosci. 2016;36(36):9391-406.
McGarry, L. M., & Carter, A. G. (2016). Inhibitory Gating of Basolateral Amygdala Inputs to the Prefrontal Cortex. The Journal of Neuroscience : the Official Journal of the Society for Neuroscience, 36(36), pp. 9391-406. doi:10.1523/JNEUROSCI.0874-16.2016.
McGarry LM, Carter AG. Inhibitory Gating of Basolateral Amygdala Inputs to the Prefrontal Cortex. J Neurosci. 2016 09 7;36(36):9391-406. PubMed PMID: 27605614.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Inhibitory Gating of Basolateral Amygdala Inputs to the Prefrontal Cortex. AU - McGarry,Laura M, AU - Carter,Adam G, PY - 2016/03/16/received PY - 2016/07/18/accepted PY - 2016/9/9/entrez PY - 2016/9/9/pubmed PY - 2017/8/18/medline KW - basolateral amygdala KW - inhibition KW - interneuron KW - prefrontal cortex KW - projection neuron KW - synapse SP - 9391 EP - 406 JF - The Journal of neuroscience : the official journal of the Society for Neuroscience JO - J. Neurosci. VL - 36 IS - 36 N2 - UNLABELLED: Interactions between the prefrontal cortex (PFC) and basolateral amygdala (BLA) regulate emotional behaviors. However, a circuit-level understanding of functional connections between these brain regions remains incomplete. The BLA sends prominent glutamatergic projections to the PFC, but the overall influence of these inputs is predominantly inhibitory. Here we combine targeted recordings and optogenetics to examine the synaptic underpinnings of this inhibition in the mouse infralimbic PFC. We find that BLA inputs preferentially target layer 2 corticoamygdala over neighboring corticostriatal neurons. However, these inputs make even stronger connections onto neighboring parvalbumin and somatostatin expressing interneurons. Inhibitory connections from these two populations of interneurons are also much stronger onto corticoamygdala neurons. Consequently, BLA inputs are able to drive robust feedforward inhibition via two parallel interneuron pathways. Moreover, the contributions of these interneurons shift during repetitive activity, due to differences in short-term synaptic dynamics. Thus, parvalbumin interneurons are activated at the start of stimulus trains, whereas somatostatin interneuron activation builds during these trains. Together, these results reveal how the BLA impacts the PFC through a complex interplay of direct excitation and feedforward inhibition. They also highlight the roles of targeted connections onto multiple projection neurons and interneurons in this cortical circuit. Our findings provide a mechanistic understanding for how the BLA can influence the PFC circuit, with important implications for how this circuit participates in the regulation of emotion. SIGNIFICANCE STATEMENT: The prefrontal cortex (PFC) and basolateral amygdala (BLA) interact to control emotional behaviors. Here we show that BLA inputs elicit direct excitation and feedforward inhibition of layer 2 projection neurons in infralimbic PFC. BLA inputs are much stronger at corticoamygdala neurons compared with nearby corticostriatal neurons. However, these inputs are even more powerful at parvalbumin and somatostatin expressing interneurons. BLA inputs thus activate two parallel inhibitory networks, whose contributions change during repetitive activity. Finally, connections from these interneurons are also more powerful at corticoamygdala neurons compared with corticostriatal neurons. Together, our results demonstrate how the BLA predominantly inhibits the PFC via a complex sequence involving multiple cell-type and input-specific connections. SN - 1529-2401 UR - https://www.unboundmedicine.com/medline/citation/27605614/Inhibitory_Gating_of_Basolateral_Amygdala_Inputs_to_the_Prefrontal_Cortex_ L2 - http://www.jneurosci.org/cgi/pmidlookup?view=long&pmid=27605614 DB - PRIME DP - Unbound Medicine ER -