Duvarci, S. & Pare, D. Amygdala microcircuits controlling learned fear. Neuron 82, 966–980 (2014).

Article  PubMed  PubMed Central  CAS  Google Scholar 

Janak, P. H. & Tye, K. M. From circuits to behaviour in the amygdala. Nature 517, 284–292 (2015).

Article  PubMed  PubMed Central  CAS  Google Scholar 

Grundemann, J. & Luthi, A. Ensemble coding in amygdala circuits for associative learning. Curr. Opin. Neurobiol. 35, 200–206 (2015).

Article  PubMed  CAS  Google Scholar 

Crosby, E. C. & Humphrey, T. Studies of the vertebrate telencephalon. II. The nuclear pattern of the anterior olfactory nucleus, tuberculum olfactorium and the amygdaloid complex in adult man. J. Comp. Neurol. 74, 309–352 (1941).

Article  Google Scholar 

Millhouse, O. E. The intercalated cells of the amygdala. J. Comp. Neurol. 247, 246–271 (1986).

Article  PubMed  CAS  Google Scholar 

Palomares-Castillo, E. et al. The intercalated paracapsular islands as a module for integration of signals regulating anxiety in the amygdala. Brain Res. 1476, 211–234 (2012).

Article  PubMed  CAS  Google Scholar 

Völsch, M. Zur vergleichenden Anatomie des Mandelkerns und seiner Nachbargebilde. Archiv. für. Mikroskopische Anat. 76, 373–523 (1910).

Article  Google Scholar 

Johnston, J. B. Further contributions to the study of the evolution of the forebrain. J. Comp. Neurol. 35, 337–481 (1923).

Article  Google Scholar 

Herry, C. et al. Neuronal circuits of fear extinction. Eur. J. Neurosci. 31, 599–612 (2010).

Article  PubMed  Google Scholar 

Pape, H. C. & Pare, D. Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear. Physiol. Rev. 90, 419–463 (2010).

Article  PubMed  CAS  Google Scholar 

Singewald, N. & Holmes, A. Rodent models of impaired fear extinction. Psychopharmacol. 236, 21–32 (2019).

Article  CAS  Google Scholar 

Maren, S. Seeking a spotless mind: extinction, deconsolidation, and erasure of fear memory. Neuron 70, 830–845 (2011).

Article  PubMed  PubMed Central  CAS  Google Scholar 

Pare, D., Quirk, G. J. & Ledoux, J. E. New vistas on amygdala networks in conditioned fear. J. Neurophysiol. 92, 1–9 (2004).

Article  PubMed  Google Scholar 

Likhtik, E., Popa, D., Apergis-Schoute, J., Fidacaro, G. A. & Pare, D. Amygdala intercalated neurons are required for expression of fear extinction. Nature 454, 642–645 (2008). By chemically lesioning the medial ITCs after training, this study provided causal evidence for a critical role for ITCs in expression of fear extinction.

Article  PubMed  PubMed Central  CAS  Google Scholar 

Berretta, S., Pantazopoulos, H., Caldera, M., Pantazopoulos, P. & Paré, D. Infralimbic cortex activation increases c-Fos expression in intercalated neurons of the amygdala. Neuroscience 132, 943–953 (2005).

Article  PubMed  CAS  Google Scholar 

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

Article  PubMed  PubMed Central  Google Scholar 

Milad, M. R. & Quirk, G. J. Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 420, 70–74 (2002).

Article  PubMed  CAS  Google Scholar 

Do-Monte, F. H., Manzano-Nieves, G., Quinones-Laracuente, K., Ramos-Medina, L. & Quirk, G. J. Revisiting the role of infralimbic cortex in fear extinction with optogenetics. J. Neurosci. 35, 3607–3615 (2015).

Article  PubMed  PubMed Central  CAS  Google Scholar 

Bukalo, O. et al. Prefrontal inputs to the amygdala instruct fear extinction memory formation. Sci. Adv. 1, e1500251 (2015).

Article  PubMed  PubMed Central  Google Scholar 

Ehrlich, I. et al. Amygdala inhibitory circuits and the control of fear memory. Neuron 62, 757–771 (2009).

Article  PubMed  CAS  Google Scholar 

Hefner, K. et al. Impaired fear extinction learning and cortico-amygdala circuit abnormalities in a common genetic mouse strain. J. Neurosci. 28, 8074–8085 (2008).

Article  PubMed  PubMed Central  CAS  Google Scholar 

Busti, D. et al. Different fear states engage distinct networks within the intercalated cell clusters of the amygdala. J. Neurosci. 31, 5131–5144 (2011). This study demonstrated differential engagement of ITCdmand ITCvmclusters in high and low fear states suggesting a new framework for their role in fear expression and extinction.

Article  PubMed  PubMed Central  CAS  Google Scholar 

Huang, C. C., Chen, C. C., Liang, Y. C. & Hsu, K. S. Long-term potentiation at excitatory synaptic inputs to the intercalated cell masses of the amygdala. Int. J. Neuropsychopharmacol. 17, 1233–1242 (2014).

Article  PubMed  CAS  Google Scholar 

Asede, D., Bosch, D., Luthi, A., Ferraguti, F. & Ehrlich, I. Sensory inputs to intercalated cells provide fear-learning modulated inhibition to the basolateral amygdala. Neuron 86, 541–554 (2015). This study showed that neurons in the ITCdmcluster receive sensory inputs and are part of fear learning-modulated feedforward and feedback inhibitory circuits controlling amygdala input and output nuclei.

Article  PubMed  CAS  Google Scholar 

Hagihara, K. M. et al. Intercalated amygdala clusters orchestrate a switch in fear state. Nature 594, 403–407 (2021). This study revealed opposing functional roles for ITCdmand ITCvmclusters and provided evidence that through mutual intercluster inhibition, ITCs enable switching between high and low fear states via connections to distinct amygdala–cortical pathways.

Article  PubMed  PubMed Central  CAS  Google Scholar 

Royer, S., Martina, M. & Paré, D. An inhibitory interface gates impulse traffic between the input and output stations of the amygdala. J. Neurosci. 19, 10575–10583 (1999).

Article  PubMed  PubMed Central  CAS  Google Scholar 

Marowsky, A., Yanagawa, Y., Obata, K. & Vogt, K. E. A specialized subclass of interneurons mediates dopaminergic facilitation of amygdala function. Neuron 48, 1025–1037 (2005). This study identified ITCs as a substrate for DA-induced amygdala disinhibition via D1 receptor-dependent hyperpolarization.

Article  PubMed  CAS  Google Scholar 

Paré, D. & Smith, Y. The intercalated cell masses project to the central and medial nuclei of the amygdala in cats. Neuroscience 57, 1077–1090 (1993).

Article  PubMed  Google Scholar 

McDonald, A. J. & Augustine, J. R. Localization of GABA-like immunoreactivity in the monkey amygdala. Neuroscience 52, 281–294 (1993).

Article  PubMed  CAS  Google Scholar 

Zikopoulos, B., John, Y. J., Garcia-Cabezas, M. A., Bunce, J. G. & Barbas, H. The intercalated nuclear complex of the primate amygdala. Neuroscience 330, 267–290 (2016).

Article  PubMed  CAS  Google Scholar 

Braak, H. & Braak, E. Neuronal types in the basolateral amygdaloid nuclei of man. Brain Res. Bull. 11, 349–365 (1983).

Article  PubMed  CAS  Google Scholar 

Urban, S. & Yilmazer-Hanke, D. M. The pigmentarchitectonic divisions and neuronal types of the central nucleus and intercalated masses of the human amygdala. J. Hirnforsch. 39, 311–319 (1999).

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