Amygdala Inputs to the Prefrontal Cortex Elicit Heterosynaptic Suppression of Hippocampal Inputs
Open accessAbstract
Whereas cooperative communication between the hippocampus (HP) and prefrontal cortex (PFC) is critical for cognitive functions, an antagonistic relationship may exist between the basolateral amygdala (BLA) and PFC during emotional processing. As PFC neurons integrate information from converging excitatory BLA and HP inputs, we explored whether the ability of BLA inputs to evoke feedforward inhibition in the PFC affects converging HP synaptic inputs using in vivo intracellular recordings in anesthetized rats. BLA train stimulation decreased HP synaptic responses in the PFC in vivo. This effect was dependent on the timing of HP-evoked responses and the strength of BLA activation. BLA train stimulation also produced heterosynaptic suppression of responses from the amygdalo-piriform cortex, an associative temporal cortical structure. Heterosynaptic suppression was unidirectional as HP trains failed to modify BLA synaptic responses. These findings provide a mechanism by which BLA activation could decrease PFC neural activity and transiently attenuate the HP influence on PFC function.
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?
Uncoupling of PFC theta oscillations from the hippocampal theta could in part be mediated by reciprocal inputs from the BLA to the PFC, which heterosynaptically suppress the influence of hippocampal inputs there.
“Uncoupling of PFC theta oscillations from the hippocampal theta could in part be mediated by reciprocal inputs from the BLA to the PFC, which heterosynaptically suppress the influence of hippocampal inputs there139.”
From Resolving the neural circuits of anxiety (2015) · cites this paper as [139]
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
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
AChE-stained horizontal sections of the rat brain in stereotaxic coordinates
Paxinos, G., WATSON, C. R. R., & Emson, P. C. (1980) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(80)90021-7 · Cited by 4,497 · see citing works
Contributions of the Amygdala to Emotion Processing: From Animal Models to Human Behavior
Phelps, E. A., & LeDoux, J. E. (2005) · Neuron · doi:10.1016/j.neuron.2005.09.025 · Cited by 3,203 · see citing works
A cortical–hippocampal system for declarative memory
Eichenbaum, H. (2000) · Nature reviews. Neuroscience · doi:10.1038/35036213 · Cited by 1,725 · see citing works
Kim, M. J., Loucks, R. A., Palmer, A. L., Brown, A. C., Solomon, K. M., Marchante, A. N., & Whalen, P. J. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.04.025 · Cited by 838 · see citing works
Prefrontal entrainment of amygdala activity signals safety in learned fear and innate anxiety
Likhtik, E., Stujenske, J. M., A Topiwala, M., Harris, A. Z., & Gordon, J. A. (2014) · Nature Neuroscience · doi:10.1038/nn.3582 · Cited by 577 · see citing works
Long-range connectivity defines behavioral specificity of amygdala neurons
Senn, V., Wolff, S. B. E., Herry, C., Grenier, F., Ehrlich, I., Gründemann, J., Fadok, J. P., Müller, C., Letzkus, J. J., & Lüthi, A. (2014) · Neuron · doi:10.1016/j.neuron.2013.11.006 · Cited by 522 · cited 2× · see citing works
“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).”
BackgroundAfferent connections of the medial frontal cortex of the rat. II. Cortical and subcortical afferents
Condé, F., Maire-Lepoivre, E., Audinat, É., & Crépel, F. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903520407 · Cited by 494 · see citing works
Chudasama, Y., & Robbins, T. W. (2006) · Biological Psychology · doi:10.1016/j.biopsycho.2006.01.005 · Cited by 484 · see citing works
Role of the Amygdala in Decision‐Making
Bechara, A., Damasio, H., & Damasio, A. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb07094.x · Cited by 475 · see citing works
Gating of Fear in Prelimbic Cortex by Hippocampal and Amygdala Inputs
Sotres-Bayón, F., Sierra‐Mercado, D., Pardilla‐Delgado, E., & Quirk, G. J. (2012) · Neuron · doi:10.1016/j.neuron.2012.09.028 · Cited by 451 · see citing works
Decision-making and impulse control after frontal lobe injuries
Bechara, A., & der Linden, M. V. (2005) · Current Opinion in Neurology · doi:10.1097/01.wco.0000194141.56429.3c · Cited by 426 · see citing works
Rosenkranz, J. A., & Grace, A. A. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-01-00324.2002 · Cited by 392 · see citing works
Kim, M. J., Gee, D. G., Loucks, R. A., Davis, F. C., & Whalen, P. J. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq237 · Cited by 388 · see citing works
Emotion processing and regulation in bipolar disorder: a review
Townsend, J. D., & Altshuler, L. L. (2012) · Bipolar Disorders · doi:10.1111/j.1399-5618.2012.01021.x · Cited by 361 · see citing works
Prefrontal Control of the Amygdala
Likhtik, E., Pelletier, J. G., Paz, R., & Paré, D. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2314-05.2005 · Cited by 361 · see citing works
Altered resting-state amygdala functional connectivity in men with posttraumatic stress disorder
Sripada, R. K., King, A. P., Garfinkel, S. N., Wang, X., Sripada, C. S., Welsh, R. C., & Liberzon, I. (2012) · Journal of Psychiatry and Neuroscience · doi:10.1503/jpn.110069 · Cited by 352 · see citing works
The amygdala modulates prefrontal cortex activity relative to conditioned fear
Garcia, R., Vouimba, R.-M., Baudry, M., & Thompson, R. F. (1999) · Nature · doi:10.1038/46286 · Cited by 347 · see citing works
Amygdala-prefrontal cortical circuitry regulates effort based decision making
Floresco, S. B., & Ghods-Sharifi, S. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhj143 · Cited by 316 · see citing works
Laviolette, S. R., Lipski, W. J., & Grace, A. A. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1168-05.2005 · Cited by 235 · see citing works
Floresco, S. B., & Tse, M. T. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.5474-06.2007 · Cited by 204 · see citing works
Influence of the hippocampus on interneurons of the rat prefrontal cortex
Tierney, P. L., Dégenètais, E., Thierry, A., Glowinski, J., & Gioanni, Y. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03501.x · Cited by 192 · see citing works
Ishikawa, A., & Nakamura, S. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-31-09987.2003 · Cited by 185 · see citing works
Oscillations and hippocampal–prefrontal synchrony
Gordon, J. A. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.02.012 · Cited by 159 · see citing works
Interactions between the prefrontal cortex and amygdala during delay discounting and reversal.
Churchwell, J. C., Morris, A. M., Heurtelou, N. M., & Kesner, R. P. (2009) · Behavioral Neuroscience · doi:10.1037/a0017734 · Cited by 141 · see citing works
Veer, I. M., Oei, N. Y. L., Spinhoven, P., van Buchem, M. A., Elzinga, B. M., & Rombouts, S. A. R. B. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.12.001 · Cited by 140 · see citing works
Subcellular Synaptic Connectivity of Layer 2 Pyramidal Neurons in the Medial Prefrontal Cortex
Little, J. P., & Carter, A. G. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1616-12.2012 · Cited by 128 · see citing works
Dégenètais, E. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.7.782 · Cited by 127 · see citing works
Pérez-Jaranay, J. M., & Vives, F. (1991) · Brain Research · doi:10.1016/0006-8993(91)91357-7 · Cited by 122 · see citing works
Functional Connectivity between Amygdala and Cingulate Cortex for Adaptive Aversive Learning
Klavir, O., Genud-Gabai, R., & Paz, R. (2013) · Neuron · doi:10.1016/j.neuron.2013.09.035 · Cited by 120 · see citing works
Amygdala inputs drive feedforward inhibition in the medial prefrontal cortex
Dilgen, J., Tejeda, H. A., & O'Donnell, P. (2013) · Journal of Neurophysiology · doi:10.1152/jn.00531.2012 · Cited by 97 · see citing works
Self-citationThomases, D. R., Cass, D. K., & Tseng, K. Y. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.4147-12.2013 · Cited by 89 · see citing works
Thomases, D. R., Cass, D. K., Meyer, J. D., Caballero, A. C., & Tseng, K. Y. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1395-14.2014 · Cited by 55 · see citing works
Closing the Gate in the Limbic Striatum: Prefrontal Suppression of Hippocampal and Thalamic Inputs
Calhoon, G. G., & O’Donnell, P. (2013) · Neuron · doi:10.1016/j.neuron.2013.01.032 · Cited by 50 · see citing works
Self-citationProjections of the Amygdalopiriform Transition Area (APir): A PHA‐L Study in the Rat
Shammah‐Lagnado, S. J., & Santiago, A. C. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb09295.x · Cited by 44 · see citing works
Esmaeili, B., & Grace, A. A. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.64 · Cited by 23 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Resolving the neural circuits of anxiety
Calhoon, G. G., & Tye, K. M. (2015) · Nature Neuroscience · doi:10.1038/nn.4101 · Cited by 766 · see citing works
Lau, T., Bigio, B., Zelli, D., McEwen, B. S., & Nasca, C. (2017) · Molecular Psychiatry · doi:10.1038/mp.2016.68 · Cited by 93 · see citing works
- Authors
- Tejeda, H. A., & O'Donnell, P.
- Affiliations
- National Institutes of Health (US)
- ORCID
- Tejeda, Hugo A.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2014-10-22
- Volume
- 34
- Issue
- 43
- Pages
- 14365-14374
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC4205558
- OpenAlex
- W2041359297
- Cited by
- 11
- References
- 36
- Citations by year
- 2025: 1 · 2024: 2 · 2023: 1 · 2022: 1 · 2019: 1 · 2018: 2 · 2017: 1 · 2016: 1 · 2015: 1
- FWCI
- 0.56
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Pfizer
- National Institutes of Health
- National Institute of Mental Health (R01MH057683)
- 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 › Neural dynamics and brain function
- Keywords
- basolateral amygdala, prefrontal cortex, hippocampus, feedforward inhibition, emotional processing, synaptic plasticity
- MeSH terms
- Amygdala, Animals, Hippocampus, Male, Neural Inhibition, Neural Pathways, Prefrontal Cortex, Excitatory Postsynaptic Potentials, Rats, Long-Evans, Rats
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