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Open AccessArticle

Optogenetic Stimulation of Prelimbic Pyramidal Neurons Maintains Fear Memories and Modulates Amygdala Pyramidal Neuron Transcriptome

1
Department of Experimental Neuroscience, IRCCS Fondazione Santa Lucia, 00143 Rome, Italy
2
Department of Systems Medicine, Tor Vergata University of Rome, 00133 Rome, Italy
3
Unit of Neurology, IRCCS Neuromed, 86077 Pozzilli, Italy
4
Department of Psychology, University “Sapienza” of Rome, 00185 Rome, Italy
5
Biological Environmental Science and Engineering Division, KAUST Environmental Epigenetics Program, Thuwal 23955-6900, Saudi Arabia
*
Author to whom correspondence should be addressed.
Int. J. Mol. Sci. 2021, 22(2), 810; https://doi.org/10.3390/ijms22020810
Received: 4 December 2020 / Revised: 12 January 2021 / Accepted: 12 January 2021 / Published: 15 January 2021
Fear extinction requires coordinated neural activity within the amygdala and medial prefrontal cortex (mPFC). Any behavior has a transcriptomic signature that is modified by environmental experiences, and specific genes are involved in functional plasticity and synaptic wiring during fear extinction. Here, we investigated the effects of optogenetic manipulations of prelimbic (PrL) pyramidal neurons and amygdala gene expression to analyze the specific transcriptional pathways associated to adaptive and maladaptive fear extinction. To this aim, transgenic mice were (or not) fear-conditioned and during the extinction phase they received optogenetic (or sham) stimulations over photo-activable PrL pyramidal neurons. At the end of behavioral testing, electrophysiological (neural cellular excitability and Excitatory Post-Synaptic Currents) and morphological (spinogenesis) correlates were evaluated in the PrL pyramidal neurons. Furthermore, transcriptomic cell-specific RNA-analyses (differential gene expression profiling and functional enrichment analyses) were performed in amygdala pyramidal neurons. Our results show that the optogenetic activation of PrL pyramidal neurons in fear-conditioned mice induces fear extinction deficits, reflected in an increase of cellular excitability, excitatory neurotransmission, and spinogenesis of PrL pyramidal neurons, and associated to strong modifications of the transcriptome of amygdala pyramidal neurons. Understanding the electrophysiological, morphological, and transcriptomic architecture of fear extinction may facilitate the comprehension of fear-related disorders. View Full-Text
Keywords: fear extinction; fear conditioning; medial prefrontal cortex; RNA sequencing; differential gene expression; electrophysiological recordings; excitatory post-synaptic currents; spinogenesis; fear-related disorders fear extinction; fear conditioning; medial prefrontal cortex; RNA sequencing; differential gene expression; electrophysiological recordings; excitatory post-synaptic currents; spinogenesis; fear-related disorders
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MDPI and ACS Style

Laricchiuta, D.; Sciamanna, G.; Gimenez, J.; Termine, A.; Fabrizio, C.; Caioli, S.; Balsamo, F.; Panuccio, A.; De Bardi, M.; Saba, L.; Passarello, N.; Cutuli, D.; Mattioni, A.; Zona, C.; Orlando, V.; Petrosini, L. Optogenetic Stimulation of Prelimbic Pyramidal Neurons Maintains Fear Memories and Modulates Amygdala Pyramidal Neuron Transcriptome. Int. J. Mol. Sci. 2021, 22, 810. https://doi.org/10.3390/ijms22020810

AMA Style

Laricchiuta D, Sciamanna G, Gimenez J, Termine A, Fabrizio C, Caioli S, Balsamo F, Panuccio A, De Bardi M, Saba L, Passarello N, Cutuli D, Mattioni A, Zona C, Orlando V, Petrosini L. Optogenetic Stimulation of Prelimbic Pyramidal Neurons Maintains Fear Memories and Modulates Amygdala Pyramidal Neuron Transcriptome. International Journal of Molecular Sciences. 2021; 22(2):810. https://doi.org/10.3390/ijms22020810

Chicago/Turabian Style

Laricchiuta, Daniela; Sciamanna, Giuseppe; Gimenez, Juliette; Termine, Andrea; Fabrizio, Carlo; Caioli, Silvia; Balsamo, Francesca; Panuccio, Anna; De Bardi, Marco; Saba, Luana; Passarello, Noemi; Cutuli, Debora; Mattioni, Anna; Zona, Cristina; Orlando, Valerio; Petrosini, Laura. 2021. "Optogenetic Stimulation of Prelimbic Pyramidal Neurons Maintains Fear Memories and Modulates Amygdala Pyramidal Neuron Transcriptome" Int. J. Mol. Sci. 22, no. 2: 810. https://doi.org/10.3390/ijms22020810

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