Neurogliaform cells of amygdala: a source of slow phasic inhibition in the basolateral complex
Open accessAbstract
Key points The amygdala is a key brain structure implicated in processing emotions and is thought to underlie anxiety‐related behaviours. Interneurons of the basolateral amygdala provide constant silencing of principal cells, and are proven to be active cellular elements during emotional processing. We report here a novel interneuron type of the amygdala, termed neurogliaform cell (NGFC), and study its function by a combination of in vivo and in vitro techniques. NGFCs provide a peculiar cell‐to‐cell form of communication via volume transmission of GABA. In‐depth analysis of specific neuron type is likely to improve the understanding of amygdala circuits in health and disease. Abstract Synaptic inhibition in the amygdala actively participates in processing emotional information. To improve the understanding of interneurons in amygdala networks it is necessary to characterize the GABAergic cell types, their connectivity and physiological roles. We used a mouse line expressing a green fluorescent protein (GFP) under the neuropeptide Y (NPY) promoter. Paired recordings between presynaptic NPY‐GFP‐expressing (+) cells and postsynaptic principal neurons (PNs) of the basolateral amygdala (BLA) were performed. The NPY‐GFP+ neurons displayed small somata and short dendrites embedded in a cloud of highly arborized axon, suggesting a neurogliaform cell (NGFC) type. We discovered that a NPY‐GFP+ cell evoked a GABA A receptor‐mediated slow inhibitory postsynaptic current (IPSC) in a PN and an autaptic IPSC. The slow kinetics of these IPSCs was likely caused by the low concentration and spillover of extracellular GABA. We also report that NGFCs of the BLA fired action potentials phase‐locked to hippocampal theta oscillations in anaesthetized rats. When this firing was re‐played in NPY+‐NGFCs in vitro , it evoked a transient depression of the IPSCs. Presynaptic GABA B receptors and functional depletion of synaptic vesicles determined this short‐term plasticity. Synaptic contacts made by recorded NGFCs showed close appositions, and rarely identifiable classical synaptic structures. Thus, we report here a novel interneuron type of the amygdala that generates volume transmission of GABA. The peculiar functional mode of NGFCs makes them unique amongst all GABAergic cell types of the amygdala identified so far.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
NG cells had not been described in BNST, but NG-like cells occur in amygdala.
“Although, to our knowledge, NG cells have not been described in the BNST before, cells with NG-like anatomy and physiology have been observed within the amygdala (Manko et al., 2012), a structure with related functional roles.”
From Single-Cell Multi-omic Integration Compares and Contrasts Features of Brain Cell Identity (2019) · cites this paper as Manko et al., 2012
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Feinleib, M., & Zar, J. H. (1975) · Journal of the American Statistical Association · doi:10.2307/2285423 · Cited by 12,671 · see citing works
Neuronal Diversity and Temporal Dynamics: The Unity of Hippocampal Circuit Operations
Klausberger, T., & Somogyi, P. (2008) · Science · doi:10.1126/science.1149381 · Cited by 2,050 · see citing works
Fritschy, J., & Mohler, H. (1995) · Journal of Comparative Neurology · doi:10.1002/cne.903590111 · Cited by 1,244 · see citing works
Pape, H.-C., & Pare, D. (2010) · Physiological Reviews · doi:10.1152/physrev.00037.2009 · Cited by 994 · see citing works
Switching on and off fear by distinct neuronal circuits
Herry, C., Ciocchi, S., Senn, V., Demmou, L., Müller, C., & Lüthi, A. (2008) · Nature · doi:10.1038/nature07166 · Cited by 950 · see citing works
Amygdala inhibitory circuits and the control of fear memory
Ehrlich, I., Humeau, Y., Grenier, F., Ciocchi, S., Herry, C., & Lüthi, A. (2009) · Neuron · doi:10.1016/j.neuron.2009.05.026 · Cited by 878 · see citing works
Amygdalar and Hippocampal Theta Rhythm Synchronization During Fear Memory Retrieval
Seidenbecher, T., Laxmi, T. R., Stork, O., & Pape, H.-C. (2003) · Science · doi:10.1126/science.1085818 · Cited by 728 · see citing works
Buhl, E. H., Halasy, K., & Somogyi, P. (1994) · Nature · doi:10.1038/368823a0 · Cited by 728 · see citing works
Pinault, D. (1996) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(95)00144-1 · Cited by 720 · see citing works
Reporting ethical matters in The Journal of Physiology: standards and advice
Drummond, G. B. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2008.167387 · Cited by 570 · see citing works
Bartos, M., Vida, I., Frotscher, M., Meyer, A. H., Monyer, H., Geiger, J. R. P., & Jónás, P. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.192233099 · Cited by 529 · see citing works
GABAB-receptor-activated K+ current in voltage-clamped CA3 pyramidal cells in hippocampal cultures.
Gähwiler, B. H., & Brown, D. A. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.5.1558 · Cited by 478 · see citing works
Drug interactions at GABAA receptors
Korpi, E. R., Gründer, G., & Lüddens, H. (2002) · Progress in Neurobiology · doi:10.1016/s0301-0082(02)00013-8 · Cited by 474 · see citing works
Klausberger, T., Márton, L. F., Baude, A., Roberts, J. D. B., Magill, P. J., & Somogyi, P. (2004) · Nature Neuroscience · doi:10.1038/nn1159 · Cited by 393 · see citing works
Airaksinen, M. S., Eilers, J., Garaschuk, O., Thoenen, H., Konnerth, A., & Meyer, M. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.4.1488 · Cited by 392 · see citing works
Regulation of cortical microcircuits by unitary GABA-mediated volume transmission
Oláh, S., Füle, M., Komlósi, G., Varga, C., Báldi, R., Barzó, P., & Tamás, G. (2009) · Nature · doi:10.1038/nature08503 · Cited by 386 · see citing works
Neurons of the lateral and basolateral amygdaloid nuclei: A golgi study in the rat
McDonald, A. J. (1982) · The Journal of Comparative Neurology · doi:10.1002/cne.902120307 · Cited by 371 · see citing works
The cellular, molecular and ionic basis of GABAA receptor signalling
Farrant, M., & Kaila, K. (2007) · Progress in brain research · doi:10.1016/s0079-6123(06)60005-8 · Cited by 369 · see citing works
Reciprocal Inhibitory Connections and Network Synchrony in the Mammalian Thalamus
Huntsman, M. M., Porcello, D. M., Homanics, G. E., DeLorey, T. M., & Huguenard, J. R. (1999) · Science · doi:10.1126/science.283.5401.541 · Cited by 361 · see citing works
Identified sources and targets of slow inhibition in the neocortex
Tamás, G., Simon, A. L., & Szabadics, J. (2003) · Science · doi:10.1126/science.1082053 · Cited by 359 · see citing works
Physiological evidence for two distinct GABAA responses in rat hippocampus
Pearce, R. A. (1993) · Neuron · doi:10.1016/0896-6273(93)90310-n · Cited by 304 · see citing works
GABAergic circuits mediate the reinforcement-related signals of striatal cholinergic interneurons
English, D. F., Ibáñez-Sandoval, O., Stark, E., Tecuapetla, F., Buzsáki, G., Deisseroth, K. A., Tepper, J. M., & Koós, T. Z. (2011) · Nature Neuroscience · doi:10.1038/nn.2984 · Cited by 288 · see citing works
Central somatostatin systems revealed with monoclonal antibodies
Vincent, S. R., McIntosh, C. H. S., Buchan, A. M. J., & Brown, J. C. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902380205 · Cited by 269 · see citing works
Paré, D., & Collins, D. R. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-07-02701.2000 · Cited by 262 · see citing works
Behavior-dependent specialization of identified hippocampal interneurons
Lapray, D., Lasztóczi, B., Lagler, M., Viney, T. J., Katona, L., Valenti, O., Hartwich, K., Borhegyi, Z., Somogyi, P., & Klausberger, T. (2012) · Nature Neuroscience · doi:10.1038/nn.3176 · Cited by 262 · see citing works
Classification of NPY-Expressing Neocortical Interneurons
Karagiannis, A., Gallopin, T., Dávid, C., Battaglia, D., Geoffroy, H., Rossier, J., Hillman, E. M. C., Staiger, J. F., & Cauli, B. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.0058-09.2009 · Cited by 256 · see citing works
Neurogliaform Neurons Form a Novel Inhibitory Network in the Hippocampal CA1 Area
Price, C. J., Cauli, B., Kovacs, E. R., Kulik, A., Lambolez, B., Shigemoto, R., & Capogna, M. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1135-05.2005 · Cited by 255 · see citing works
Self-citationFuentealba, P., Begum, R., Capogna, M., Jinno, S., Márton, L. F., Csicsvari, J., Thomson, A., Somogyi, P., & Klausberger, T. (2008) · Neuron · doi:10.1016/j.neuron.2008.01.034 · Cited by 255 · see citing works
Self-citationSajdyk, T. J., Vandergriff, M. G., & Gehlert, D. R. (1999) · European Journal of Pharmacology · doi:10.1016/s0014-2999(99)00018-7 · Cited by 241 · see citing works
Kubota, Y., Shigematsu, N., Karube, F., Sekigawa, A., Kato, S., Yamaguchi, N., Hirai, Y., Morishima, M., & Kawaguchi, Y. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq252 · Cited by 235 · see citing works
Physiological Role of Calcium-Activated Potassium Currents in the Rat Lateral Amygdala
Faber, E. S. L., & Sah, P. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-05-01618.2002 · Cited by 234 · see citing works
Makkar, S., Zhang, S., & Cranney, J. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.53 · Cited by 232 · see citing works
Interneurons in the basolateral amygdala
Spampanato, J. G., Polepalli, J. S., & Sah, P. (2010) · Neuropharmacology · doi:10.1016/j.neuropharm.2010.11.006 · Cited by 205 · see citing works
Networks of Parvalbumin-Positive Interneurons in the Basolateral Amygdala
Woodruff, A. R., & Sah, P. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3686-06.2007 · Cited by 205 · see citing works
Activation of AMPA, Kainate, and Metabotropic Receptors at Hippocampal Mossy Fiber Synapses
Min, M., Rusakov, D. A., & Kullmann, D. M. (1998) · Neuron · doi:10.1016/s0896-6273(00)80566-8 · Cited by 199 · see citing works
Vida, I., Halasy, K., Szinyei, C., Somogyi, P., & Buhl, E. H. (1998) · The Journal of Physiology · doi:10.1111/j.1469-7793.1998.755bv.x · Cited by 190 · see citing works
Szabadics, J., Tamás, G., & Soltesz, I. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0707204104 · Cited by 170 · see citing works
Prenosil, G., Gasser, E. M. S., Rudolph, U., Keist, R., Fritschy, J., & Vogt, K. E. (2006) · Journal of Neurophysiology · doi:10.1152/jn.01199.2005 · Cited by 169 · see citing works
Bienvenu, T., Busti, D., Magill, P. J., Ferraguti, F., & Capogna, M. (2012) · Neuron · doi:10.1016/j.neuron.2012.04.022 · Cited by 168 · see citing works
Self-citationThe Synaptic Basis of GABAA,slow
Banks, M. I., Li, T.-B., & Pearce, R. A. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-04-01305.1998 · Cited by 166 · see citing works
RO4938581, a novel cognitive enhancer acting at GABAA α5 subunit-containing receptors
Ballard, T. M., Knoflach, F., Prinssen, E. P. M., Borroni, E., Vivian, J. A., Basile, J., Gasser, R., Moreau, J., Wettstein, J. G., Buettelmann, B., et al. (2008) · Psychopharmacology · doi:10.1007/s00213-008-1357-7 · Cited by 156 · see citing works
McDonald, A. J., & Mascagni, F. (2002) · Brain Research · doi:10.1016/s0006-8993(02)02650-1 · Cited by 152 · see citing works
A Novel Functionally Distinct Subtype of Striatal Neuropeptide Y Interneuron
Ibáñez-Sandoval, O., Tecuapetla, F., Ünal, B., Shah, F., Koós, T. Z., & Tepper, J. M. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2628-11.2011 · Cited by 150 · see citing works
Synapse Density Regulates Independence at Unitary Inhibitory Synapses
Overstreet, L. S., & Westbrook, G. L. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-07-02618.2003 · Cited by 148 · see citing works
Cell type‐ and synapse‐specific variability in synaptic GABAA receptor occupancy
Hájos, N., Nusser, Z., Rancz, E. A., Freund, T. F., & Módy, I. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00964.x · Cited by 145 · see citing works
GABAA,slow: causes and consequences
Capogna, M., & Pearce, R. A. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2010.10.005 · Cited by 129 · see citing works
Self-citationWozny, C., & Williams, S. R. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq257 · Cited by 129 · see citing works
Output of neurogliaform cells to various neuron types in the human and rat cerebral cortex
Oláh, S. (2007) · Frontiers in Neural Circuits · doi:10.3389/neuro.04.004.2007 · Cited by 118 · see citing works
Fuentealba, P., Klausberger, T., Karayannis, T., Suen, W. Y., Huck, J., Tomioka, R., Rockland, K., Capogna, M., Studer, M., Morales, M., et al. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4199-09.2010 · Cited by 113 · see citing works
Self-citationGABAB Receptor Modulation of Feedforward Inhibition through Hippocampal Neurogliaform Cells
Price, C. J., Scott, R., Rusakov, D. A., & Capogna, M. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.4673-07.2008 · Cited by 107 · see citing works
Self-citationMcDonald, A. J. (1989) · Brain Research · doi:10.1016/0006-8993(89)90297-7 · Cited by 107 · see citing works
Nusser, Z., Naylor, D. E., & Módy, I. (2001) · Biophysical Journal · doi:10.1016/s0006-3495(01)76101-2 · Cited by 100 · see citing works
Microcircuits Mediating Feedforward and Feedback Synaptic Inhibition in the Piriform Cortex
Suzuki, N., & Bekkers, J. M. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.4112-11.2012 · Cited by 94 · see citing works
Kapur, A., Pearce, R. A., Lytton, W. W., & Haberly, L. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.78.5.2531 · Cited by 91 · see citing works
Microscopic Kinetics and Energetics Distinguish GABAA Receptor Agonists from Antagonists
Jones, M. V., Jónás, P., Sahara, Y., & Westbrook, G. L. (2001) · Biophysical Journal · doi:10.1016/s0006-3495(01)75909-7 · Cited by 87 · see citing works
Armstrong, C., Szabadics, J., Tamás, G., & Soltesz, I. (2011) · Journal of Comparative Neurology · doi:10.1002/cne.22577 · Cited by 86 · see citing works
Karayannis, T., Elfant, D., Huerta-Ocampo, I., Teki, S., Scott, R. S., Rusakov, D. A., Jones, M. V., & Capogna, M. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.5883-09.2010 · Cited by 85 · see citing works
Self-citationIvy/neurogliaform interneurons coordinate activity in the neurogenic niche
Markwardt, S. J., Dieni, C. V., Wadiche, J. I., & Overstreet-Wadiche, L. (2011) · Nature Neuroscience · doi:10.1038/nn.2935 · Cited by 82 · see citing works
Crowley, J. J., Fioravante, D., & Regehr, W. G. (2009) · Neuron · doi:10.1016/j.neuron.2009.09.004 · Cited by 74 · see citing works
Pan, B., Dong, Y., Ito, W., Yanagawa, Y., Shigemoto, R., & Morozov, A. (2009) · Neuron · doi:10.1016/j.neuron.2009.01.029 · Cited by 73 · see citing works
Sosulina, L., Schwesig, G., Seifert, G., & Pape, H. (2008) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2008.08.002 · Cited by 60 · see citing works
Barberis, A., Petrini, E. M., & Mozrzymas, J. W. (2011) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2011.00006 · Cited by 60 · see citing works
Prenosil, G. A. (2006) · Journal of Neurophysiology · doi:10.1152/jn.01199.2006 · Cited by 60 · see citing works
Heterogeneous Kinetics and Pharmacology of Synaptic Inhibition in the Chick Auditory Brainstem
Kuo, S. P., Bradley, L. A., & Trussell, L. O. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0103-09.2009 · Cited by 58 · see citing works
GABA Affinity Shapes IPSCs in Thalamic Nuclei
Schofield, C. M., & Huguenard, J. R. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0377-07.2007 · Cited by 57 · see citing works
McDonald, A. J., Payne, D., & Mascagni, F. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90185-i · Cited by 55 · see citing works
Vargas‐Caballero, M., Martin, L. J., Salter, M. W., Orser, B. A., & Paulsen, O. (2009) · Neuropharmacology · doi:10.1016/j.neuropharm.2009.11.005 · Cited by 52 · see citing works
A golgi study of the amygdaloid complex in the cat.
Tömböl, T., & Szafrańska-Kosmal, A. (1972) · PubMed · Cited by 51 · see citing works
Gaudreau, H., & Paré, D. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.75.3.1301 · Cited by 45 · see citing works
Altered GABAA,slowInhibition and Network Oscillations in Mice Lacking the GABAAReceptor β3Subunit
Hentschke, H., Benkwitz, C., Banks, M. I., Perkins, M. G., Homanics, G. E., & Pearce, R. A. (2009) · Journal of Neurophysiology · doi:10.1152/jn.00651.2009 · Cited by 43 · see citing works
Constantinople, C. M., Disney, A. A., Maffie, J. K., Rudy, B., & Hawken, M. J. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22111 · Cited by 38 · see citing works
Neurons of the basolateral amygdala: A Golgi study in the opossum (Didelphis virginiana)
McDonald, A. J., & Culberson, J. L. (1981) · American Journal of Anatomy · doi:10.1002/aja.1001620404 · Cited by 38 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Single-Cell Multi-omic Integration Compares and Contrasts Features of Brain Cell Identity
Welch, J. D., Kozareva, V., Ferreira, A., Vanderburg, C., Martin, C., & Macosko, E. Z. (2019) · Cell · doi:10.1016/j.cell.2019.05.006 · Cited by 1,193 · see citing works
Bocchio, M., Nabavi, S., & Capogna, M. (2017) · Neuron · doi:10.1016/j.neuron.2017.03.022 · Cited by 259 · see citing works
Self-citationNeurodevelopment, GABA System Dysfunction, and Schizophrenia
Schmidt, M. J., & Mirnics, K. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.95 · Cited by 239 · see citing works
Heterogeneity and Diversity of Striatal GABAergic Interneurons: Update 2018
Tepper, J. M., Koós, T. Z., Ibáñez-Sandoval, O., Tecuapetla, F., Faust, T. W., & Assous, M. (2018) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2018.00091 · Cited by 218 · see citing works
Serotonin, Amygdala and Fear: Assembling the Puzzle
Bocchio, M., McHugh, S. B., Bannerman, D. M., Sharp, T., & Capogna, M. (2016) · Frontiers in Neural Circuits · doi:10.3389/fncir.2016.00024 · Cited by 207 · see citing works
Self-citationImpact of Basal Forebrain Cholinergic Inputs on Basolateral Amygdala Neurons
Ünal, Ç. T., Paré, D., & Záborszky, L. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.2706-14.2015 · Cited by 124 · see citing works
The role of Neuropeptide Y in fear conditioning and extinction
Tasan, R. O., Verma, D., Wood, J. C., Lach, G., Hörmer, B. A., de Lima, T. C. M., Herzog, H., & Sperk, G. (2015) · Neuropeptides · doi:10.1016/j.npep.2015.09.007 · Cited by 117 · see citing works
Herd, M. B., Brown, A. R., Lambert, J. J., & Belelli, D. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.1174-13.2013 · Cited by 85 · see citing works
GABAergic cell type diversity in the basolateral amygdala
Capogna, M. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.01.006 · Cited by 82 · see citing works
Self-citationVereczki, V., Veres, J. M., Müller, K., Nagy, G. A., Rácz, B., Barsy, B., & Hájos, N. (2016) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2016.00020 · Cited by 77 · see citing works
Bazelot, M., Bocchio, M., Kasugai, Y., Fischer, D., Dodson, P. D., Ferraguti, F., & Capogna, M. (2015) · Neuron · doi:10.1016/j.neuron.2015.08.024 · Cited by 77 · see citing works
Self-citationNeurogliaform cells dynamically regulate somatosensory integration via synapse-specific modulation
Chittajallu, R., Pelkey, K. A., & McBain, C. J. (2013) · Nature Neuroscience · doi:10.1038/nn.3284 · Cited by 73 · see citing works
Functional neuroanatomy of the basolateral amygdala: Neurons, neurotransmitters, and circuits
McDonald, A. (2020) · Handbook of Behavioral Neuroscience · doi:10.1016/b978-0-12-815134-1.00001-5 · Cited by 73 · see citing works
Phasic, Nonsynaptic GABA-A Receptor-Mediated Inhibition Entrains Thalamocortical Oscillations
Rovó, Z., Mátyás, F., Barthó, P., Slézia, A., Lecci, S., Pellegrini, C., Astori, S., Dávid, C., Hangya, B., Lüthi, A., et al. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.4386-13.2014 · Cited by 73 · see citing works
Deficient tonic GABAergic conductance and synaptic balance in the fragile X syndrome amygdala
Martin, B. S., Corbin, J. G., & Huntsman, M. M. (2014) · Journal of Neurophysiology · doi:10.1152/jn.00597.2013 · Cited by 69 · see citing works
Interneuron Types and Their Circuits in the Basolateral Amygdala
Hájos, N. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.687257 · Cited by 61 · see citing works
Total Number and Ratio of GABAergic Neuron Types in the Mouse Lateral and Basal Amygdala
Vereczki, V., Müller, K., Krizsán, É., Máté, Z., Fekete, Z., Rovira-Esteban, L., Veres, J. M., Erdélyi, F., & Hájos, N. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.2700-20.2021 · Cited by 60 · see citing works
Veres, J. M., Nagy, G. A., & Hájos, N. (2017) · eLife · doi:10.7554/elife.20721 · Cited by 58 · see citing works
Bocchio, M., Fucsina, G., Oikonomidis, L., McHugh, S. B., Bannerman, D. M., Sharp, T., & Capogna, M. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.157 · Cited by 54 · see citing works
Self-citationCraig, M. T., & McBain, C. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.10.002 · Cited by 56 · see citing works
Rhomberg, T., Rovira-Esteban, L., Vikór, A., Paradiso, E., Kremser, C., Nagy-Pál, P., Papp, O. I., Tasan, R. O., Erdélyi, F., Szabó, G., et al. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.2063-17.2018 · Cited by 43 · see citing works
Integrative inference of brain cell similarities and differences from single-cell genomicsPreprint
Welch, J. D., Kozareva, V., Ferreira, A. N., Vanderburg, C. R., Martin, C., & Macosko, E. Z. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/459891 · Cited by 40 · see citing works
Grünewald, B., Lange, M. D., Werner, C. D., O’Leary, A., Weishaupt, A., Popp, S., Pearce, D. A., Wiendl, H., Reif, A., Pape, H., et al. (2017) · eLife · doi:10.7554/elife.28685 · Cited by 38 · see citing works
Morphological and physiological properties of CCK/CB1R-expressing interneurons in the basal amygdala
Rovira-Esteban, L., Péterfi, Z., Vikór, A., Máté, Z., Szabó, G., & Hájos, N. (2017) · Brain Structure and Function · doi:10.1007/s00429-017-1417-z · Cited by 31 · see citing works
The hippocampus associated GABAergic neural network impairment in early-stage of Alzheimer's disease
Tang, Y., Yan, Y., Mao, J., Ni, J., & Qing, H. (2023) · Ageing Research Reviews · doi:10.1016/j.arr.2023.101865 · Cited by 34 · see citing works
Rovira-Esteban, L., Gunduz‐Cinar, O., Bukalo, O., Limoges, A., Brockway, E. T., Müller, K., Fenno, L. E., Kim, Y. S., Ramakrishnan, C., Andrási, T., et al. (2019) · eNeuro · doi:10.1523/eneuro.0220-19.2019 · Cited by 32 · see citing works
Inhibitory Circuits in the Basolateral Amygdala in Aversive Learning and Memory
Perumal, M. B., & Sah, P. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.633235 · Cited by 31 · see citing works
Inhibitory circuits in fear memory and fear-related disorders
Singh, S. P., & Topolnik, L. (2023) · Frontiers in Neural Circuits · doi:10.3389/fncir.2023.1122314 · Cited by 29 · see citing works
Crane, J. W., Holmes, N. M., Fam, J. P., Westbrook, R. F., & Delaney, A. (2019) · Journal of Neurophysiology · doi:10.1152/jn.00571.2019 · Cited by 23 · see citing works
Wang, X., Guo, J., Song, Y., Wang, Q., Hu, S., Gou, L., & Gao, Y. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00251 · Cited by 22 · see citing works
Rees, C. L., White, C. M., & Ascoli, G. A. (2017) · Current Medicinal Chemistry · doi:10.2174/0929867324666170414163506 · Cited by 20 · see citing works
Sleep and Serotonin Modulate Paracapsular Nitric Oxide Synthase Expressing Neurons of the Amygdala
Bocchio, M., Fisher, S. P., Ünal, G., Ellender, T. J., Vyazovskiy, V. V., & Capogna, M. (2016) · eNeuro · doi:10.1523/eneuro.0177-16.2016 · Cited by 17 · see citing works
Self-citationWang, X., Liu, C., Wang, X., Gao, F., & Zhan, R. (2017) · Brain Research · doi:10.1016/j.brainres.2017.02.009 · Cited by 14 · see citing works
Veres, J. M., Fekete, Z., Müller, K., Andrási, T., Rovira-Esteban, L., Barabás, B., Papp, O. I., & Hájos, N. (2023) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2023.1120338 · Cited by 12 · see citing works
Fu, X., & Tasker, J. G. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1421617 · Cited by 10 · see citing works
Ozsvár, A., Komlósi, G., Oláh, G., Baka, J., Molnár, G., & Tamás, G. (2021) · eLife · doi:10.7554/elife.65634 · Cited by 10 · see citing works
BLA-involved circuits in neuropsychiatric disorders
Ma, L., Li, S., Jiao, X., Li, Z., Zhou, Y. X., Zhou, C.-R., Zhou, C.-R., Zheng, H., & Wu, Y.-Q. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102363 · Cited by 9 · see citing works
McDonald, A. J., & Augustine, J. R. (2019) · The Journal of Comparative Neurology · doi:10.1002/cne.24785 · Cited by 9 · see citing works
Retzlaff, C. L., & Rothwell, P. E. (2022) · Neuropharmacology · doi:10.1016/j.neuropharm.2022.109212 · Cited by 8 · see citing works
Serotonergic control of GABAergic inhibition in the lateral amygdala
Yamamoto, R., Furuyama, T., Sugai, T., Ono, M., Paré, D., & Kato, N. (2019) · Journal of Neurophysiology · doi:10.1152/jn.00500.2019 · Cited by 8 · see citing works
Christie, B. R., Gross, A., Willoughby, A., Gräfe, E. L., Brand, J., Bosdachin, E., Reid, H. M. O., Acosta, C., & Eyolfson, E. (2023) · Journal of Visualized Experiments · doi:10.3791/64592 · Cited by 7 · see citing works
A combinatory genetic strategy for targeting neurogliaform neurons in the mouse basolateral amygdala
Ozsvár, A., Sieburg, M. C., Sietam, M. D., Hou, W., & Capogna, M. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1254460 · Cited by 5 · see citing works
Self-citationNeuropeptide Y and amygdala circuitry: Modulation of stress-related behavior
Urban, J. H. (2020) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-815134-1.00007-6 · Cited by 3 · see citing works
Sources of GABA That Activate Extrasynaptic GABAA Receptors
Bright, D. P., Houston, C. M., & Brickley, S. G. (2014) · The Receptors · doi:10.1007/978-1-4939-1426-5_6 · Cited by 1 · see citing works
Functioning of the Core Neural Network in Fear and Extinction
Bennett, M. R., & Lagopoulos, J. (2018) · Springer eBooks · doi:10.1007/978-3-319-91116-8_6 · Cited by 1 · see citing works
Marco Capogna, a pioneering neuroscientist and true European
Ferraguti, F., Fredes, F., Hou, W., Somogyi, P., & Thompson, S. (2023) · European Journal of Neuroscience · doi:10.1111/ejn.15950
Schwert, H., Salur, E., Richard, M., Pöllmann, M., Lesch, K., Asan, E., & Schmitt-Böhrer, A. G. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.10.07.680627
A time-delay model of dopamine-modulated prefrontal–limbic interactions in schizophrenia
Kaslik, É., Matei, M. R., Neamţu, M., & Rǎdulescu, A. (2025) · Chaos Solitons & Fractals · doi:10.1016/j.chaos.2025.117606
Schwert, H., Salur, E., Richard, M., Pöllmann, M., Lesch, K., Asan, E., & Schmitt-Böhrer, A. G. (2026) · Journal of Neural Transmission · doi:10.1007/s00702-026-03224-x
- Authors
- Mańko, M., Bienvenu, T. C. M., Dalezios, Y., & Capogna, M.
- Affiliations
- University of Oxford (GB)
- University of Crete (GR)
- Corresponding author
- Capogna, Marco
- Venue
- The Journal of Physiology
- Publisher
- Wiley
- Published
- 2012-10-19
- Volume
- 590
- Issue
- 22
- Pages
- 5611-5627
- ISSN
- 0022-3751 (ISSN-L)
- 1469-7793
- PMC
- PMC3528981
- OpenAlex
- W2156185464
- Cited by
- 51
- References
- 71
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 3 · 2023: 5 · 2022: 1 · 2021: 4 · 2020: 2 · 2019: 5 · 2018: 5 · 2017: 6 · 2016: 3 · 2015: 4 · 2014: 6 · 2013: 2 · 2012: 1
- FWCI
- 1.71
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The Journal of Physiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Institut National de la Santé et de la Recherche Médicale
- Medical Research Council
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- neurogliaform cells, basolateral amygdala, GABAergic interneurons, GABAA receptor, GABAB receptors, synaptic depression, hippocampal theta oscillations, neuropeptide Y, anxiety, synaptic inhibition
- MeSH terms
- Action Potentials, Amygdala, Animals, Axons, Dendrites, gamma-Aminobutyric Acid, Interneurons, Synaptic Transmission, Neuronal Plasticity, Synapses, Theta Rhythm, GABA Antagonists, Rats, Inhibitory Postsynaptic Potentials, GABAergic Neurons
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
