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Long-Range Connectivity Defines Behavioral Specificity of Amygdala Neurons
Open accessAbstract
Memories are acquired and encoded within large-scale neuronal networks spanning different brain areas. The anatomical and functional specificity of such long-range interactions and their role in learning is poorly understood. The amygdala and the medial prefrontal cortex (mPFC) are interconnected brain structures involved in the extinction of conditioned fear. Here, we show that a defined subpopulation of basal amygdala (BA) projection neurons targeting the prelimbic (PL) subdivision of mPFC is active during states of high fear, whereas BA neurons targeting the infralimbic (IL) subdivision are recruited, and exhibit cell-type-specific plasticity, during fear extinction. Pathway-specific optogenetic manipulations demonstrate that the activity balance between pathways is causally involved in fear extinction. Together, our findings demonstrate that, although intermingled locally, long-range connectivity defines distinct subpopulations of amygdala projection neurons and indicate that the formation of long-term extinction memories depends on the balance of activity between two defined amygdala-prefrontal pathways.
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“There is evidence to suggest that there is a dorso-ventral topographic segregation of BLA input to the mPFC; more dorsal projections (to PL) encode threat-stimulating information while more ventral projections (to IL) encode threat extinction-related information [51].”
From Prefrontal cortex, amygdala, and threat processing: implications for PTSD (2022) · cites this paper as [51]
In the citing paper
“Moreover, optogenetic excitation of BLA→dmPFC PNs has been shown to increase conditioned fear after extinction (19).”
From Chronic Stress Remodels Synapses in an Amygdala Circuit-Specific Manner (2019) · cites this paper as [19]
In the citing paper
“By contrast, extinction of the learned fear association increases activity in basal amygdala neurons targeting the infralimbic cortex105.”
From Resolving the neural circuits of anxiety (2015) · cites this paper as [105]
In the citing paper
“During auditory fear conditioning, activity in basal amygdala neurons projecting to the prelimbic cortex is increased105”
From Resolving the neural circuits of anxiety (2015) · cites this paper as [105]
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“This demarcation is noteworthy given that PL-projecting and IL-projecting BA neurons have differential roles in fear and extinction 81 .”
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“A balance of activities between the PL and IL appears to be important for the expression and suppression of threat memories [53,54].”
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“…has been implicated in aversive processing and goal-directed behaviors, whereas ventral mPFC (vmPFC) has been more often associated with the formation and expression of extinction behaviors and habit (Ostlund and Balleine, 2005; Sotres-Bayon and Quirk, 2010; Senn et al., 2014; Sun et al., 2018).”
BackgroundMultinode implementation of an extended Hodgkin–Huxley simulator
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“Those very same neurons (the IL-projecting BLA neurons) are found to be active during fear extinction [53], underscoring the observation that orexin activation in the lateral hypothalamus (LH) accounts for individual differences in fear extinction [47].”
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“Functionally, BLA is mainly known as a processing hub for the amygdaloid complex by receiving various sensory and associative information from the brainstem, thalamus and the cortex and integrating this information to allow for a proper amygdala response [34, 45].”
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“Moreover, not all GABAergic interneurons within a population have been found to participate in these neural processes (Bienvenu et al., 2012; Wolff et al., 2014; Krabbe et al., 2019).”
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“…have much in common with Pavlovian fear conditioning (Bouton et al., 2001; Bremner et al., 2008; Graham and Milad, 2011; LeDoux, 2000; Maren and Quirk, 2004; Pitman et al., 1999; Shin et al., 2006; Sullivan et al., 2003) and are conserved across species (LeDoux, 2014; Phelps and LeDoux, 2005).”
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“For instance, recent work has demonstrated that intermingled BLA neuron populations that project either to the prelimbic or infralimbic PFC are implicated in mediating the expression and extinction of conditioned fear responses, respectively (Senn et al., 2014).”
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“Photo-stimulation of the BLA-PL projection increased freezing, while activation of BLA-IL neurons contributed to fear-extinction (Senn et al, 2014; Burgos-Robles et al., 2017).”
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“141 Neurofilament light chain, a neurofilament protein and cyto-skeletal component in long myelinated axons, can be used as a peripheral marker of neuroaxonal injury, and was increased in and associated with reduced cognitive performance in depressed patients.”
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“Specifically, it has extensive connections to the amygdala for the regulation of aberrant emotions (Senn et al., 2014; Zhang et al., 2019).”
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Neural Circuits for Fear Relapse
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“basolateral amygdala (BLA) have been similarly implicated in extinction learning [21].”
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“Such broadening of spike width has also been reported in infralimbic PFC neurons projecting to the amygdala in response to extinction training (Senn et al., 2014).”
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“This is in line with neuroimaging studies of PTSD patients, in which loss of inhibitory control resulting from mPFC hypoactivation, has been suggested to cause hyperactivation of the amygdala and hippocampal atrophy (Shin et al., 2006; Kamiya and Abe, 2020).”
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“Plasticity in the form of long-term potentiation at thalamocortical-basolateral amygdala synapses is required for both the acquisition and expression of conditioned fear, and distinct subpopulations of basolateral neurons seem to either facilitate (“fear on” neurons) or inhibit (“fear off” neurons) fear responding via…”
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Zhu, L., Zhu, L., Huang, Y., Shi, W., & Yu, B. (2018) · Neuroreport · doi:10.1097/wnr.0000000000001069 · Cited by 6
Sex-dependent fear memory impairment in cocaine-sired rat offspring
Rich, M. T., Worobey, S. J., Mankame, S., Pang, Z. P., Swinford-Jackson, S. E., & Pierce, R. C. (2023) · Science Advances · doi:10.1126/sciadv.adf6039 · Cited by 6
“Interestingly and perhaps unexpectedly, BLA fear neurons project to the prelimbic cortex, whereas BLA extinction neurons target the infralimbic cortex ( 45 ).”
Fast and slow extinction pathways in defensive survival circuits
Orederu, T. A., & Schiller, D. (2018) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2018.06.004 · Cited by 6
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Neuromodulatory signaling contributing to the encoding of aversion
Wu, C.-H., Camelot, L., Lecca, S., & Mameli, M. (2025) · Trends in Neurosciences · doi:10.1016/j.tins.2025.04.003 · Cited by 6
“Neurons in the amygdala also innervate the infralimbic and prelimbic areas of the prefrontal cortex where they contribute to fear learning and fear extinction [33].”
Synaptic organization and associative learning-related activity of basolateral amygdala interneurons
Báldi, R., Muthuswamy, S., Yasmin, F., Quadir, S. G., Zaidi, D., Kwon, M., Kandil, I. F., Johnson, K., Loomba, N., & Patel, S. (2025) · Cell Reports · doi:10.1016/j.celrep.2025.116295 · Cited by 5
Heterogeneous plasticity of amygdala interneurons in associative learning and extinction
Favila, N., Marsico, J. C., Pacheco, C. M., Kenet, S., Escribano, B., Bitterman, Y., Gründemann, J., Lüthi, A., & Krabbe, S. (2025) · Nature Communications · doi:10.1038/s41467-025-66122-y · Cited by 7
“This inhibitory plasticity can for example stabilise memory traces or increase the selectivity of engrams 32 , or enhance the contrast between distinct long-range PN circuits associated with fear or extinction states 22,33 .”
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“Research indicates that the basolateral amygdala ’ s (BLA) input to the PL encodes information that stimulates threat perception (Senn et al., 2014) while synaptic connections between these regions strengthen in response to stress (Marcus et al., 2020).”
Periaqueductal gray activates antipredatory neural responses in the amygdala of foraging rats
Kim, E. J., Kong, M.-S., Park, S., Cho, J., & Kim, J. J. (2024) · eLife · doi:10.7554/elife.88733.4 · Cited by 5
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“To target the callosally projecting neurons specifically could have been achieved using a more advanced injection strategy—for instance with dependent viral expression (Lima et al., 2009; Yizhar et al., 2011; Senn et al., 2014), using e.”
MethodHartsock, M. J., Brennan, N. A., & Spencer, R. L. (2022) · Journal of Biological Rhythms · doi:10.1177/07487304221128161 · Cited by 5
“, 2021), amygdala (Senn et al., 2014; Hagihara et al., 2021), or prelimbic prefrontal cortex (Marek et al.”
BackgroundJing, L., Ma, C., Xu, L., & Richter‐Levin, G. (2023) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyad054 · Cited by 5
“…direct input from a subgroup of basolateral amygdala neurons and being required for the expression of conditioned fear, while the basolateral amygdala–infralimbic projection is vital for fear extinction (Corcoran and Quirk, 2007; Senn et al., 2014; Tovote et al., 2015; Roelofs and Dayan, 2022).”
BackgroundHartsock, M. J., Levy, C. T., Navarro, M. J., Saddoris, M. P., & Spencer, R. L. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.0878-24.2024 · Cited by 6
Optogenetics: illuminating the neural bases of rodent behavior
Lobo, M. K., Francis, C., & Chaudhury, D. (2014) · Open Access Animal Physiology · doi:10.2147/oaap.s42339 · Cited by 6
“More recently, herpes simplex virus or canine adenoviruses were utilized to deliver Cre to afferent axons and brain regions to allow for subsequent injection of opsin vectors in upstream cell bodies.(24,43) These viruses provide a novel way of localizing and dissecting region specific afferent activity into a brain ar…”
Connecting the dots between cell populations, whole-brain activity, and behavior
Beloate, L. N., & Zhang, N. (2022) · Neurophotonics · doi:10.1117/1.nph.9.3.032208 · Cited by 5
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MouseCircuits.org: An online repository to guide the circuit era of disordered affectPreprint
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Metadata
- Authors
- Senn, V., Wolff, S. B. E., Herry, C., Grenier, F., Ehrlich, I., Gründemann, J., Fadok, J. P., Müller, C., Letzkus, J. J., & Lüthi, A.
- Affiliations
- University of Basel (CH)
- Friedrich Miescher Institute (CH)
- Corresponding author
- Lüthi, Andreas
- ORCID
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2014-01
- Volume
- 81
- Issue
- 2
- Pages
- 428-437
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W1977502547
- Cited by
- 522
- References
- 38
- Citations by year
- 2026: 17 · 2025: 28 · 2024: 35 · 2023: 35 · 2022: 40 · 2021: 55 · 2020: 45 · 2019: 52 · 2018: 55 · 2017: 47 · 2016: 30 · 2015: 49 · 2014: 34
- FWCI
- 29.74
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Funders
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Keywords
- amygdala, medial prefrontal cortex, fear extinction, long-range connectivity, prelimbic cortex, infralimbic cortex, memory extinction, optogenetic manipulation, fear conditioning
- MeSH terms
- Channelrhodopsins, Acoustic Stimulation, Action Potentials, Amygdala, Analysis of Variance, Animals, Bacterial Proteins, Biophysics, Cell Count, Conditioning, Classical, Elapid Venoms, Electric Stimulation, Extinction, Psychological, Fear, Hippocampus, Light, Luminescent Proteins, Male, Neural Pathways, Neurons, Peptides, Time Factors, Oncogene Proteins v-fos, Prefrontal Cortex, Herpesvirus 1, Human, Patch-Clamp Techniques, Mice, Biophysical Phenomena, Optogenetics, In Vitro Techniques
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