Prefrontal inputs to the amygdala instruct fear extinction memory formation

American Psychiatric Association DSM-5 Diagnostic and Statistical Manual of Mental Disorders (APA Press Washington DC ed. 4 2013).

A. Holmes, N. Singewald, Individual differences in recovery from traumatic fear. Trends Neurosci. 36, 23–31 (2013).

R. R. Rozeske, S. Valerio, F. Chaudun, C. Herry, Prefrontal neuronal circuits of contextual fear conditioning. Genes Brain Behav. 14, 22–36 (2015).

10.1016/j.neuron.2014.04.042

10.1146/annurev.psych.121208.131631

A. Lüthi, C. Lüscher, Pathological circuit function underlying addiction and anxiety disorders. Nat. Neurosci. 17, 1635–1643 (2014).

J. M. Stafford, D. K. Maughan, E. C. Ilioi, K. M. Lattal, Exposure to a fearful context during periods of memory plasticity impairs extinction via hyperactivation of frontal-amygdalar circuits. Learn. Mem. 20, 156–163 (2013).

10.1038/nn.3869

C. A. Orsini, S. Maren, Neural and cellular mechanisms of fear and extinction memory formation. Neurosci. Biobehav. Rev. 36, 1773–1802 (2012).

10.1016/j.nlm.2013.11.002

M. Maroun, A. Kavushansky, A. Holmes, C. Wellman, H. Motanis, Enhanced extinction of aversive memories by high-frequency stimulation of the rat infralimbic cortex. PLOS One 7, e35853 (2012).

10.1101/lm.306106

10.1016/j.neuron.2013.09.025

T. Amano, C. T. Unal, D. Paré, Synaptic correlates of fear extinction in the amygdala. Nat. Neurosci. 13, 489–494 (2010).

A. Amir, T. Amano, D. Pare, Physiological identification and infralimbic responsiveness of rat intercalated amygdala neurons. J. Neurophysiol. 105, 3054–3066 (2011).

10.1002/cne.20738

A. J. McDonald, F. Mascagni, L. Guo, Projections of the medial and lateral prefrontal cortices to the amygdala: A Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience 71, 55–75 (1996).

10.1016/j.conb.2010.02.005

10.1016/j.celrep.2015.02.008

Y. Smith, J. F. Paré, D. Paré, Differential innervation of parvalbumin-immunoreactive interneurons of the basolateral amygdaloid complex by cortical and intrinsic inputs. J. Comp. Neurol. 416, 496–508 (2000).

10.1016/0304-3940(95)12212-5

10.1002/syn.10279

C. R. Pinard, F. Mascagni, A. J. McDonald, Medial prefrontal cortical innervation of the intercalated nuclear region of the amygdala. Neuroscience 205, 112–124 (2012).

D. Busti, R. Geracitano, N. Whittle, Y. Dalezios, M. Mańko, W. Kaufmann, K. Sätzler, N. Singewald, M. Capogna, F. Ferraguti, Different fear states engage distinct networks within the intercalated cell clusters of the amygdala. J. Neurosci. 31, 5131–5144 (2011).

10.1016/j.neuroscience.2009.12.004

10.1038/nature09820

10.1038/nature12041

10.1523/JNEUROSCI.3137-14.2015

10.1038/nature01138

S. C. Kim, Y. S. Jo, I. H. Kim, H. Kim, J. S. Choi, Lack of medial prefrontal cortex activation underlies the immediate extinction deficit. J. Neurosci. 30, 832–837 (2010).

A. Holmes, P. J. Fitzgerald, K. P. MacPherson, L. DeBrouse, G. Colacicco, S. M. Flynn, S. Masneuf, K. E. Pleil, C. Li, C. A. Marcinkiewcz, T. L. Kash, O. Gunduz-Cinar, M. Camp, Chronic alcohol remodels prefrontal neurons and disrupts NMDAR-mediated fear extinction encoding. Nat. Neurosci. 15, 1359–1361 (2012).

10.1073/pnas.1202087109

10.1101/lm.1474609

10.1038/npp.2010.184

K. Jüngling, T. Seidenbecher, L. Sosulina, J. Lesting, S. Sangha, S. D. Clark, N. Okamura, D. M. Duangdao, Y. L. Xu, R. K. Reinscheid, H. C. Pape, Neuropeptide S-mediated control of fear expression and extinction: Role of intercalated GABAergic neurons in the amygdala. Neuron 59, 298–310 (2008).

J. C. Repa, J. Muller, J. Apergis, T. M. Desrochers, Y. Zhou, J. E. LeDoux, Two different lateral amygdala cell populations contribute to the initiation and storage of memory. Nat. Neurosci. 4, 724–731 (2001).

10.1038/nature07166

N. Singewald, C. Schmuckermair, N. Whittle, A. Holmes, K. J. Ressler, Pharmacology of cognitive enhancers for exposure-based therapy of fear, anxiety and trauma-related disorders. Pharmacol. Ther. 149, 150–190 (2015).

10.1038/nature05744

10.3389/fnsys.2011.00018

10.1038/nprot.2011.413

A. V. Kravitz, S. F. Owen, A. C. Kreitzer, Optogenetic identification of striatal projection neuron subtypes during in vivo recordings. Brain Res. 1511, 21–32 (2013).

R. Ammari, C. Lopez, B. Bioulac, L. Garcia, C. Hammond, Subthalamic nucleus evokes similar long lasting glutamatergic excitations in pallidal, entopeduncular and nigral neurons in the basal ganglia slice. Neuroscience 166, 808–818 (2010).

P. F. Fitzgerald, C. R. Pinard, M. C. Camp, M. Feyder, A. Sah, H. C. Bergstrom, C. Graybeal, Y. Liu, O. M. Schlüter, S. G. Grant, N. Singewald, W. Xu, A. Holmes, Durable fear memories require PSD-95. Mol. Psychiatry 20, 901–912 (2015).

N. Whittle, M. Hauschild, G. Lubec, A. Holmes, N. Singewald, Rescue of impaired fear extinction and normalization of cortico-amygdala circuit dysfunction in a genetic mouse model by dietary zinc restriction. J. Neurosci. 30, 13586–13596 (2010).

K. Hefner, N. Whittle, J. Juhasz, M. Norcross, R. M. Karlsson, L. M. Saksida, T. J. Bussey, N. Singewald, A. Holmes, Impaired fear extinction learning and cortico-amygdala circuit abnormalities in a common genetic mouse strain. J. Neurosci. 28, 8074–8075 (2008).