Cannabinoid transmission in the basolateral amygdala modulates fear memory formation via functional inputs to the prelimbic cortex

Tan, Huibing; Lauzon, Nicole M.; Bishop, Stephanie F.; Chi, Ning; Bechard, Melanie; Laviolette, Steven R.

doi:10.1523/jneurosci.4718-10.2011

Cited by 92Cannabis and Cannabinoid ResearchMemory and Neural MechanismsNeuroscience and Neuropharmacology Research

Cannabinoid transmission in the basolateral amygdala modulates fear memory formation via functional inputs to the prelimbic cortex

Open access

Tan, Huibing, Lauzon, Nicole M., Bishop, Stephanie F., Chi, Ning, Bechard, Melanie, Laviolette, Steven R.·2011·The Journal of Neuroscience

DOI 10.1523/jneurosci.4718-10.2011PMC PMC6622725

Open this paper in CoChat — free account Open PDF

Abstract

The cannabinoid CB1 receptor system is critically involved in the control of associative fear memory formation within the amygdala-prefrontal cortical pathway. The CB1 receptor is found in high concentrations in brain structures that are critical for emotional processing, including the basolateral amygdala (BLA) and the prelimbic division (PLC) of the medial prefrontal cortex (mPFC). However, the precise role of CB1 receptor transmission within the BLA during the processing of fear memory is not fully understood. We examined the potential role of BLA CB1 receptor transmission during an olfactory fear-conditioning procedure in rats by pharmacologically modulating CB1 cannabinoid transmission directly within the BLA. We report that blockade of BLA CB1 receptor transmission prevents the acquisition of associative fear memory, while having no effect on the recall or consolidation of these memories. In contrast, intra-BLA activation of CB1 receptor transmission or blockade of endocannabinoid reuptake strongly potentiated the emotional salience of normally subthreshold fear-conditioning stimuli. In addition, pharmacological inactivation of the mPFC before intra-BLA CB1 activation blocked CB1-receptor-mediated potentiation of fear memory formation. In vivo single-unit electrophysiological recordings within the PLC revealed that modulation of BLA CB1 receptor transmission strongly influences neuronal activity within subpopulations of PLC neurons, with blockade of intra-BLA CB1 receptor transmission inhibiting spontaneous PLC neuronal activity and activation of CB1 receptors producing robust activation, in terms of neuronal firing frequency and bursting activity. Thus, cannabinoid transmission within the BLA strongly modulates the processing of associative fear memory via functional interactions with PLC neuronal populations.

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

Crossref · 10.1523/jneurosci.4718-10.2011

Cites

30 of 30 references verified0 citation errors · 0 not checkable

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?

Responses to fear cues in mPFC neurons receiving inputs from BLA were potentiated by the CB1R agonist WIN55212-2, and CB1R blockade/inverse agonism with AM251 in these regions disrupts fear learning and learning-related long-term potentiation.
“Responses to fear cues in mPFC neurons receiving inputs from BLA were potentiated by the CB1R agonist WIN55212-2, and CB1R blockade/inverse agonism (with AM251) in these regions disrupts fear learning and learning-related synaptic plasticity (long-term potentiation) [83–85].”
From Amygdala FAAH and anandamide: mediating protection and recovery from stress (2013) · cites this paper as [84]
The effects of ECBs on fear are not restricted to the BLA but involve a pathway between the BLA and mPFC.
“These effects on fear are not restricted to the BLA but involve a pathway between the BLA and mPFC.”
From Amygdala FAAH and anandamide: mediating protection and recovery from stress (2013) · cites this paper as [84]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

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
Cannabinoid receptor localization in brain.
Herkenham, M., Lynn, A. B., Little, M. D., Johnson, M. R., Melvin, L. S., de Costa, B. R., & Rice, K. C. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.5.1932 · Cited by 2,321 · see citing works
The endogenous cannabinoid system controls extinction of aversive memories
Marsicano, G., Wotjak, C. T., Azad, S. C., Bisogno, T., Rammes, G., Cascio, M. G., Hermann, H., Tang, J., Hofmann, C., Zieglgänsberger, W., et al. (2002) · Nature · doi:10.1038/nature00839 · Cited by 1,728 · see citing works
Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system
Tsou, K., Brown, S., Sañudo-Peña, M. C., Mackie, K., & Walker, J. M. (1998) · Neuroscience · doi:10.1016/s0306-4522(97)00436-3 · Cited by 1,586 · see citing works
The Amygdala: a functional analysis
Aggleton, J. P. (2000) · Cited by 964 · see citing works
Distribution of CB1 cannabinoid receptors in the amygdala and their role in the control of GABAergic transmission
Katona, I., Rancz, E. A., Acsády, L., Ledent, C., Mackie, K., Hájos, N., & Freund, T. F. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-23-09506.2001 · Cited by 668 · cited 1× · see citing works
“Within the BLA, CB1 receptors are found on inhibitory local GABAergic interneurons, but are absent in the adjacent central nucleus (Herkenham et al., 1990; Tsou et al., 1998; Katona et al., 2001).”
Background
Cellular Mechanisms of Infralimbic and Prelimbic Prefrontal Cortical Inhibition and Dopaminergic Modulation of Basolateral Amygdala Neurons In Vivo
Rosenkranz, J., & Grace, A. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-01-00324.2002 · Cited by 422 · see citing works
The Prefrontal Cortex Regulates Lateral Amygdala Neuronal Plasticity and Responses to Previously Conditioned Stimuli
Rosenkranz, J. A., Moore, H., & Grace, A. A. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-35-11054.2003 · Cited by 344 · see citing works
Puberty as a highly vulnerable developmental period for the consequences of cannabis exposure
Schneider, M. (2008) · Addiction Biology · doi:10.1111/j.1369-1600.2008.00110.x · Cited by 330 · see citing works
Endocannabinoids in the rat basolateral amygdala enhance memory consolidation and enable glucocorticoid modulation of memory
Campolongo, P., Roozendaal, B., Trezza, V., Hauer, D., Schelling, G., McGaugh, J. L., & Cuomo, V. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900835106 · Cited by 294 · see citing works
Circuitry for associative plasticity in the amygdala involves endocannabinoid signaling
Azad, S. C., Monory, K., Marsicano, G., Cravatt, B. F., Lutz, B., Zieglgänsberger, W., & Rammes, G. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.2134-04.2004 · Cited by 263 · cited 4× · see citing works
“…BLA neuronal population would be expected to increase local inhibitory feedback on BLA projection neurons, as suggested by other neuronal recording studies that have observed strong inhibition of BLA interneurons after application of CB1 receptor agonists (Azad et al., 2004; Pistis et al., 2004).”
BackgroundResultInfluential
A Subpopulation of Neurons in the Medial Prefrontal Cortex Encodes Emotional Learning with Burst and Frequency Codes through a Dopamine D4Receptor-Dependent Basolateral Amygdala Input
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
Self-citation
The Amygdala
(2000) · doi:10.1093/oso/9780198505013.001.0001 · Cited by 229 · see citing works
Activation of the cannabinoid receptor type 1 decreases glutamatergic and GABAergic synaptic transmission in the lateral amygdala of the mouse
Azad, S. C., Eder, M., Marsicano, G., Lutz, B., Zieglgänsberger, W., & Rammes, G. (2003) · Learning & Memory · doi:10.1101/lm.53303 · Cited by 220 · see citing works
Dopaminergic Regulation of Inhibitory and Excitatory Transmission in the Basolateral Amygdala–Prefrontal Cortical Pathway
Floresco, S. B., & Tse, M. T. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.5474-06.2007 · Cited by 204 · see citing works
Construction and analysis of non-Poisson stimulus-response models of neural spiking activity
Barbieri, R., Quirk, M. C., Frank, L. M., Wilson, M. A., & Brown, E. N. (2001) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(00)00344-7 · Cited by 200 · see citing works
Direct Actions of Cannabinoids on Synaptic Transmission in the Nucleus Accumbens: A Comparison With Opioids
Hoffman, A. F., & Lupica, C. R. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.85.1.72 · Cited by 194 · see citing works
Cannabinoids potentiate emotional learning plasticity in neurons of the medial prefrontal cortex through basolateral amygdala inputs
Laviolette, S. R., & Grace, A. A. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0707-06.2006 · Cited by 189 · see citing works
Self-citation
The roles of cannabinoid and dopamine receptor systems in neural emotional learning circuits: implications for schizophrenia and addiction
Laviolette, S. R., & Grace, A. A. (2006) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-006-6027-5 · Cited by 170 · see citing works
Self-citation
Localization of the CB1 type cannabinoid receptor in the rat basolateral amygdala: high concentrations in a subpopulation of cholecystokinin-containing interneurons
McDonald, A. J., & Mascagni, F. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00380-3 · Cited by 157 · cited 3× · see citing works
“Within the BLA, high concentrations of CB1 receptors are found localized on inhibitory interneurons (McDonald and Mascagni, 2001).”
Background
Discriminative fear conditioning to context expressed by multiple measures of fear in the rat
Antoniadis, E. A., & McDonald, R. J. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(98)00056-4 · Cited by 151 · see citing works
Amygdala input monosynaptically innervates parvalbumin immunoreactive local circuit neurons in rat medial prefrontal cortex
Gabbott, P. L. A., Warner, T., & Busby, S. J. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.01.026 · Cited by 133 · see citing works
Cannabinoids modulate neuronal firing in the rat basolateral amygdala: evidence for CB1- and non-CB1-mediated actions.
Pistis, M., Perra, S., Pillolla, G., Melis, M., Gessa, G., & Muntoni, A. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2003.08.003 · Cited by 124 · see citing works
Cannabinoids inhibit GABAergic synaptic transmission in mice nucleus accumbens
Manzoni, O. J., & Bockaert, J. (2001) · European Journal of Pharmacology · doi:10.1016/s0014-2999(01)00723-3 · Cited by 103 · see citing works
Cannabis use and brain structural alterations in first episode schizophrenia — A region of interest, voxel based morphometric study
Bangalore, S. S., Prasad, K. M. R., Montrose, D. M., Goradia, D. D., Diwadkar, V. A., & Keshavan, M. S. (2008) · Schizophrenia Research · doi:10.1016/j.schres.2007.11.029 · Cited by 100 · see citing works
Cannabis, Cannabinoids and Schizophrenia: Integration of the Evidence
Cohen, M. A., Solowij, N., & Carr, V. J. (2008) · Australian & New Zealand Journal of Psychiatry · doi:10.1080/00048670801961156 · Cited by 90 · see citing works
The effect of CB<sub>1</sub> receptor antagonism in the right basolateral amygdala on conditioned fear and associated analgesia in rats
Roche, M., O'Connor, E., Diskin, C., & Finn, D. P. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05861.x · Cited by 83 · see citing works
Integrated cannabinoid CB1 receptor transmission within the amygdala–prefrontal cortical pathway modulates neuronal plasticity and emotional memory encoding
Tan, H., Lauzon, N. M., Bishop, S. F., Bechard, M. A., & Laviolette, S. R. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhp210 · Cited by 81 · see citing works
Self-citation
Dopamine D1versus D4Receptors Differentially Modulate the Encoding of Salient versus Nonsalient Emotional Information in the Medial Prefrontal Cortex
Lauzon, N. M., Bishop, S. F., & Laviolette, S. R. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0178-09.2009 · Cited by 66 · see citing works
Self-citation

Flagged first, then by citations

Sorted by citations

The endocannabinoid system and the brain.
Mechoulam, R., & Parker, L. A. (2013) · Annual Review of Psychology · doi:10.1146/annurev-psych-113011-143739 · Cited by 1,090 · see citing works
Neurobiological Interactions Between Stress and the Endocannabinoid System
Morena, M., Patel, S., Bains, J. S., & Hill, M. N. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.166 · Cited by 663 · see citing works
Convergent translational evidence of a role for anandamide in amygdala-mediated fear extinction, threat processing and stress-reactivity
Gunduz-Cinar, O., MacPherson, K. P., Cinar, R., Gamble-George, J., Sugden, K., Williams, B., Godlewski, G., Ramikie, T. S., Gorka, A. X., Alapafuja, S. O., et al. (2013) · Molecular Psychiatry · doi:10.1038/mp.2012.72 · Cited by 307 · see citing works
Amygdala FAAH and anandamide: mediating protection and recovery from stress
Gunduz-Cinar, O., Hill, M. N., McEwen, B. S., & Holmes, A. (2013) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2013.08.008 · Cited by 229 · see citing works
Prefrontal cortical regulation of fear learning
Gilmartin, M. R., Balderston, N. L., & Helmstetter, F. J. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2014.05.004 · Cited by 197 · see citing works
Endogenous cannabinoid release within prefrontal-limbic pathways affects memory consolidation of emotional training
Morena, M., Roozendaal, B., Trezza, V., Ratano, P., Peloso, A., Hauer, D., Atsak, P., Trabace, L., Cuomo, V., McGaugh, J. L., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1420285111 · Cited by 146 · see citing works
The endocannabinoid system: An emotional buffer in the modulation of memory function
Morena, M., & Campolongo, P. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.12.010 · Cited by 143 · see citing works
Annual research review: on the developmental neuropsychology of substance use disorders
J. Conrod, P., & Nikolaou, K. (2016) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.12516 · Cited by 137 · see citing works
Adolescent THC Exposure Causes Enduring Prefrontal Cortical Disruption of GABAergic Inhibition and Dysregulation of Sub-Cortical Dopamine Function
Renard, J., Szkudlarek, H. J., Kramar, C. P., Jobson, C. E. L., Moura, K., Rushlow, W. J., & Laviolette, S. R. (2017) · Scientific Reports · doi:10.1038/s41598-017-11645-8 · Cited by 125 · see citing works
Self-citation
Endocannabinoid System: the Direct and Indirect Involvement in the Memory and Learning Processes—a Short Review
Kruk-Słomka, M., Dzik, A., Budzyńska, B., & Biała, G. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-0313-5 · Cited by 107 · see citing works
Bimodal Control of Fear-Coping Strategies by CB 1 Cannabinoid Receptors
Metna‐Laurent, M., Gómez, E. S., Verrier, D., Conforzi, M., Jégo, P., Lafenêtre, P., & Marsicano, G. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1054-12.2012 · Cited by 104 · see citing works
The Neurobiological Bases of Memory Formation: From Physiological Conditions to Psychopathology
Bisaz, R., Travaglia, A., & Alberini, C. M. (2014) · Psychopathology · doi:10.1159/000363702 · Cited by 109 · see citing works
Role of the endocannabinoid system in regulating glucocorticoid effects on memory for emotional experiences
Atsak, P., Roozendaal, B., & Campolongo, P. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2011.08.047 · Cited by 98 · see citing works
Cannabinoids and emotionality: a neuroanatomical perspective
McLaughlin, R. J., & Gobbi, G. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.07.052 · Cited by 82 · see citing works
The Role of Cannabinoid Transmission in Emotional Memory Formation: Implications for Addiction and Schizophrenia
Tan, H., Ahmad, T., Loureiro, M., Zunder, J. S., & Laviolette, S. R. (2014) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2014.00073 · Cited by 72 · see citing works
Self-citation
Involvement of cannabinoid receptors in the amygdala and prefrontal cortex of rats in fear learning, consolidation, retrieval and extinction
Kuhnert, S., Meyer, C., & Koch, M. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.05.002 · Cited by 67 · see citing works
The Lateral Habenula Directs Coping Styles Under Conditions of Stress via Recruitment of the Endocannabinoid System
Berger, A. L., Henricks, A. M., Lugo, J. M., Wright, H. R., Warrick, C. R., Sticht, M. A., Morena, M., Río, I. B., Laredo, S. A., Craft, R. M., et al. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.04.018 · Cited by 66 · see citing works
Cannabinoid Transmission in the Prefrontal Cortex Bi-Phasically Controls Emotional Memory Formation via Functional Interactions with the Ventral Tegmental Area
Draycott, B., Loureiro, M., Ahmad, T., Tan, H., Zunder, J. S., & Laviolette, S. R. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1297-14.2014 · Cited by 63 · see citing works
Self-citation
Endocannabinoid signaling in the amygdala: anatomy, synaptic signaling, behavior, and adaptations to stress
Ramikie, T. S., & Patel, S. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2011.08.037 · Cited by 62 · see citing works
A cortico-amygdala neural substrate for endocannabinoid modulation of fear extinction
Gunduz-Cinar, O., Castillo, L. I., Xia, M.-Y., Leer, E. V., Brockway, E. T., Pollack, G. A., Yasmin, F., Bukalo, O., Limoges, A., Oreizi-Esfahani, S., et al. (2023) · Neuron · doi:10.1016/j.neuron.2023.06.023 · Cited by 54 · see citing works
The Endocannabinoid System and Anxiety
Lisboa, S. F. D. S., Gomes, F. V., Terzian, A. L. B., de Aguiar, D. C., Moreira, F. A., Resstel, L. B. M., & Guimarães, F. S. (2016) · Vitamins and hormones · doi:10.1016/bs.vh.2016.09.006 · Cited by 56 · see citing works
Cannabinoid Transmission in the Hippocampus Activates Nucleus Accumbens Neurons and Modulates Reward and Aversion-Related Emotional Salience
Loureiro, M., Kramar, C. P., Renard, J., Rosen, L. G., & Laviolette, S. R. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.10.016 · Cited by 54 · see citing works
Self-citation
Cannabinoid Transmission in the Prelimbic Cortex Bidirectionally Controls Opiate Reward and Aversion Signaling through Dissociable Kappa Versus μ-Opiate Receptor Dependent Mechanisms
Ahmad, T., Lauzon, N. M., Jaeger, X. D., & Laviolette, S. R. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.1686-13.2013 · Cited by 53 · see citing works
Self-citation
The neural circuits and molecular mechanisms underlying fear dysregulation in posttraumatic stress disorder
Iqbal, J., Huang, G.-D., Xue, Y.-X., Yang, M., & Jia, X. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1281401 · Cited by 49 · see citing works
The CB1 Receptor Antagonist AM251 Impairs Reconsolidation of Pavlovian Fear Memory in the Rat Basolateral Amygdala
Ratano, P., Everitt, B. J., & Milton, A. L. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.103 · Cited by 49 · see citing works
The endocannabinoid transport inhibitor AM404 differentially modulates recognition memory in rats depending on environmental aversiveness
Campolongo, P., Ratano, P., Manduca, A., Scattoni, M. L., Palmery, M., Trezza, V., & Cuomo, V. (2012) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2012.00011 · Cited by 48 · see citing works
Cannabinoid CB1 receptors in the dorsal hippocampus and prelimbic medial prefrontal cortex modulate anxiety-like behavior in rats: Additional evidence
Lisboa, S. F. D. S., Borges, A. A., Nejo, P., Fassini, A., Guimarães, F. S., & Resstel, L. B. M. (2015) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2015.01.005 · Cited by 43 · see citing works
Lights on Endocannabinoid-Mediated Synaptic Potentiation
Piette, C., Cui, Y., Gervasi, N., & Venance, L. (2020) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2020.00132 · Cited by 40 · see citing works
CB1 receptors in the formation of the different phases of memory-related processes in the inhibitory avoidance test in mice
Kruk-Słomka, M., & Biała, G. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.12.023 · Cited by 37 · see citing works
Systemic or intra-prelimbic cortex infusion of prazosin impairs fear memory reconsolidation
Monte, F. H. D., de Souza, R. R., Wong, T., & Carobrez, A. P. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.01.031 · Cited by 36 · see citing works
Correlations between the Memory-Related Behavior and the Level of Oxidative Stress Biomarkers in the Mice Brain, Provoked by an Acute Administration of CB Receptor Ligands
Kruk-Słomka, M., Boguszewska‐Czubara, A., Słomka, T., Budzyńska, B., & Biała, G. (2015) · Neural Plasticity · doi:10.1155/2016/9815092 · Cited by 37 · see citing works
Seeing through the smoke: Human and animal studies of cannabis use and endocannabinoid signalling in corticolimbic networks
Silveira, M. M., Arnold, J. C., Laviolette, S. R., Hillard, C. J., Celorrio, M., Aymerich, M. S., & Adams, W. K. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.09.007 · Cited by 36 · see citing works
Self-citation
Molecular and neuronal plasticity mechanisms in the amygdala-prefrontal cortical circuit: implications for opiate addiction memory formation
Rosen, L. G., Sun, N., Rushlow, W. J., & Laviolette, S. R. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00399 · Cited by 34 · see citing works
Self-citation
Regional changes in the type 1 cannabinoid receptor are associated with cognitive dysfunction in Parkinson’s disease
Ceccarini, J., Casteels, C., Ahmad, R. U., Crabbé, M., de Vliet, L. V., Vanhaute, H., Vandenbulcke, M., Vandenberghe, W., & Laere, K. V. (2019) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-019-04445-x · Cited by 31 · see citing works
Endocannabinoid signaling and memory dynamics: A synaptic perspective
Drumond, A., Madeira, N., & Fonseca, R. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.07.031 · Cited by 27 · see citing works
Canabinoides ajudam a desvendar aspectos etiológicos em comum e trazem esperança para o tratamento de autismo e epilepsia
Malcher‐Lopes, R. (2014) · Revista da Biologia · doi:10.7594/revbio.13.01.07 · Cited by 29 · see citing works
Supra-normal stimulation of dopamine D1 receptors in the prelimbic cortex blocks behavioral expression of both aversive and rewarding associative memories through a cyclic-AMP-dependent signaling pathway
Lauzon, N. M., Bechard, M., Ahmad, T., & Laviolette, S. R. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.10.029 · Cited by 27 · see citing works
Self-citation
l-Theanine Prevents Long-Term Affective and Cognitive Side Effects of Adolescent Δ-9-Tetrahydrocannabinol Exposure and Blocks Associated Molecular and Neuronal Abnormalities in the Mesocorticolimbic Circuitry
Felice, M. D., Renard, J., Hudson, R., Szkudlarek, H. J., Pereira, B. J. G., Schmid, S., Rushlow, W. J., & Laviolette, S. R. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.1050-20.2020 · Cited by 26 · see citing works
Self-citation
Cannabinoid functions in the amygdala contribute to conditioned fear memory in streptozotocin-induced diabetic mice: Interaction with glutamatergic functions
Ikeda, H., Ikegami, M., Kai, M., & Kamei, J. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2015.04.012 · Cited by 26 · see citing works
Cannabinoid modulation of memory consolidation within the cerebellum
Steinmetz, A. B., & Freeman, J. H. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.11.002 · Cited by 24 · see citing works
Remote memories are enhanced by COMT activity through dysregulation of the endocannabinoid system in the prefrontal cortex
Scheggia, D., Zamberletti, E., Realini, N., Mereu, M., Contarini, G., Ferretti, V., Managò, F., Margiani, G., Brunoro, R., Rubino, T., et al. (2017) · Molecular Psychiatry · doi:10.1038/mp.2017.126 · Cited by 24 · see citing works
Lateral habenula cannabinoid CB1 receptor involvement in drug-associated impulsive behavior
Zapata, A. G., & Lupica, C. R. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108604 · Cited by 22 · see citing works
Distinct neuronal activation patterns are associated with PCP-induced social withdrawal and its reversal by the endocannabinoid-enhancing drug URB597
Matricon, J., Seillier, A., & Giuffrida, A. (2016) · Neuroscience Research · doi:10.1016/j.neures.2016.04.004 · Cited by 22 · see citing works
The role of catecholamines in modulating responses to stress: Sex‐specific patterns, implications, and therapeutic potential for post‐traumatic stress disorder and opiate withdrawal
Ross, J. A., & Bockstaele, E. J. V. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14714 · Cited by 19 · see citing works
Glucocorticoid-endocannabinoid uncoupling mediates fear suppression deficits after early – Life stress
Atsak, P., Morena, M., Schoenmaker, C., Tabak, E., Oomen, C. A., Jamil, S., Hill, M. N., & Roozendaal, B. (2018) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.02.021 · Cited by 22 · see citing works
How do stupendous cannabinoids modulate memory processing via affecting neurotransmitter systems?
Vaseghi, S., Nasehi, M., & Zarrindast, M. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.10.018 · Cited by 21 · see citing works
Effect of the Endocannabinoid System in Memory Updating and Forgetting
Lunardi, P. S., Souza, L. W., dos Santos, B. D., Popik, B., & Alvares, L. D. O. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.07.045 · Cited by 20 · see citing works
Cannabinoid receptor-1 signaling contributions to sign-tracking and conditioned reinforcement in rats
Bacharach, S. Z., Nasser, H. M., Zlebnik, N. E., Dantrassy, H. M., Kochli, D. E., Gyawali, U., Cheer, J. F., & Calu, D. J. (2018) · Psychopharmacology · doi:10.1007/s00213-018-4993-6 · Cited by 19 · see citing works
Increased mGlu5 mRNA expression in BLA glutamate neurons facilitates resilience to the long-term effects of a single predator scent stress exposure
Shallcross, J., Wu, L., Wilkinson, C. S., Knackstedt, L. A., & Schwendt, M. (2021) · Brain Structure and Function · doi:10.1007/s00429-021-02326-4 · Cited by 18 · see citing works
Medial prefrontal cortex circuit function during retrieval and extinction of associative learning under anesthesia
Fenton, G. E., Halliday, D. M., Mason, R., & Stevenson, C. W. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.01.028 · Cited by 18 · see citing works
Opiate exposure state controls dopamine D3 receptor and cdk5/calcineurin signaling in the basolateral amygdala during reward and withdrawal aversion memory formation
Rosen, L. G., Rushlow, W. J., & Laviolette, S. R. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.06.009 · Cited by 18 · see citing works
Self-citation
Targeting the Endocannabinoid System in Borderline Personality Disorder: Corticolimbic and Hypothalamic Perspectives
Ferber, S. G., Hazani, R., Shoval, G., & Weller, A. (2020) · Current Neuropharmacology · doi:10.2174/1570159x18666200429234430 · Cited by 16 · see citing works
Identification of a novel fatty acid binding protein-5-CB2 receptor-dependent mechanism regulating anxiety behaviors in the prefrontal cortex
Uzuneser, T. C., Szkudlarek, H. J., Jones, M., Nashed, M. G., Clement, T., Wang, H., Ojima, I., Rushlow, W. J., & Laviolette, S. R. (2022) · Cerebral Cortex · doi:10.1093/cercor/bhac220 · Cited by 15 · see citing works
Self-citation
Adolescent traumatic stress experience results in less robust conditioned fear and post-extinction fear cue responses in adult rats
Moore, N. L. T., Gauchan, S., & Genovese, R. F. (2014) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2014.01.011 · Cited by 15 · see citing works
The influence of self-awareness on emotional memory formation: an fMRI study
Pais-Vieira, C., Wing, E. A., & Cabeza, R. E. L. (2015) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsv141 · Cited by 15 · see citing works
Delta‐9‐tetrahydrocannabinol potentiates fear memory salience through functional modulation of mesolimbic dopaminergic activity states
Fitoussi, A., Zunder, J. S., Tan, H., & Laviolette, S. R. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.13951 · Cited by 15 · see citing works
Self-citation
The role of endocannabinoids in consolidation, retrieval, reconsolidation, and extinction of fear memory
Mizuno, I., & Matsuda, S. (2021) · Pharmacological Reports · doi:10.1007/s43440-021-00246-y · Cited by 15 · see citing works
Endocannabinoid interactions in the regulation of acquisition of contextual conditioned fear
Balogh, Z., Szente, L., Bíró, L., Varga, Z. K., Haller, J., & Aliczki, M. (2018) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2018.11.007 · Cited by 14 · see citing works
Cannabinoid reward and aversion effects in the posterior ventral tegmental area are mediated through dissociable opiate receptor subtypes and separate amygdalar and accumbal dopamine receptor substrates
Ahmad, T., & Laviolette, S. R. (2017) · Psychopharmacology · doi:10.1007/s00213-017-4669-7 · Cited by 13 · see citing works
Self-citation
Modulation of the effects of the cannabinoid agonist, ACPA, on spatial and non-spatial novelty detection in mice by dopamine D1 receptor drugs infused into the basolateral amygdala
Mohammadi, M., Nasehi, M., & Zarrindast, M. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.11.003 · Cited by 12 · see citing works
Effects of Cannabis and Cannabinoids in the Human Nervous System
Kalant, H. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-418679-8.00013-7 · Cited by 11 · see citing works
The endocannabinoid system in social anxiety disorder: from pathophysiology to novel therapeutics
Ahmed, M., Boileau, I., Le Foll, B., Carvalho, A. F., & Kloiber, S. (2022) · Brazilian Journal of Psychiatry · doi:10.1590/1516-4446-2021-1926 · Cited by 11 · see citing works
Neuronal protein-tyrosine phosphatase 1B hinders sensory-motor functional recovery and causes affective disorders in two different focal ischemic stroke models
Stewart, A. F. R., Chen, H., Cruz, S. A., Qin, Z., & Ricke, K. M. (2020) · Neural Regeneration Research · doi:10.4103/1673-5374.286970 · Cited by 10 · see citing works
Memory Consolidation Depends on Endogenous Hippocampal Levels of Anandamide: CB1 and M4, but Possibly not TRPV1 Receptors Mediate AM404 effects
Scienza-Martin, K., Lotz, F. N., Zanona, Q. K., Santana, F., Crestani, A. P., Boos, F. Z., Calcagnotto, M. E., & Quillfeldt, J. A. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.04.009 · Cited by 10 · see citing works
CB1 receptor antagonism in capuchin monkeys alters social interaction and aversive memory extinction
Gonczarowska, N., Tomaz, C. A. B., Caixeta, F. V., Malcher‐Lopes, R., Barros, M., Nishijo, H., & Maior, R. S. (2019) · Psychopharmacology · doi:10.1007/s00213-019-05305-0 · Cited by 10 · see citing works
Inhibition of fatty acid binding protein-5 in the basolateral amygdala induces anxiolytic effects and accelerates fear memory extinction
Jones, M. J., Uzuneser, T. C., Clement, T., Wang, H., Ojima, I., Rushlow, W. J., & Laviolette, S. R. (2023) · Psychopharmacology · doi:10.1007/s00213-023-06468-7 · Cited by 9 · see citing works
Self-citation
Interactions Between the Ubiquitin–Proteasome System, Nrf2, and the Cannabinoidome as Protective Strategies to Combat Neurodegeneration: Review on Experimental Evidence
Monsalvo-Maraver, L. Á., Ovalle-Noguez, E. A., Nava-Osorio, J., Maya-López, M., Rangel‐López, E., Túnez, I., Tinkov, A. A., Tizabi, Y., Aschner, M., Santamarı́a, A., et al. (2024) · Neurotoxicity Research · doi:10.1007/s12640-024-00694-3 · Cited by 8 · see citing works
Restoration of CB1 receptor function in hippocampal GABAergic neurons rescues memory deficits in Huntington’s disease models
Franco, N. D., de Tena, I. B., Sánchez-Ruiz, A., Pereda-Velarde, A., Enfedaque, F., González-Arias, C., Miquel-Rio, L., Bortolozzi, A. A., Rodríguez‐Puertas, R., Costas‐Insua, C., et al. (2025) · Translational Neurodegeneration · doi:10.1186/s40035-025-00500-w · Cited by 8 · see citing works
Systemic or intra-amygdala infusion of an endocannabinoid CB1 receptor antagonist AM251 blocked propofol-induced anterograde amnesia
Ren, Y., Wang, J., Xu, P., Xu, Y.-J., & Miao, C. H. (2014) · Neuroscience Letters · doi:10.1016/j.neulet.2014.11.001 · Cited by 7 · see citing works
Cannabinoid regulation of opiate motivational processing in the mesolimbic system: the integrative roles of amygdala, prefrontal cortical and ventral hippocampal input pathways
Laviolette, S. R. (2016) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2016.10.004 · Cited by 6 · see citing works
Self-citation
Lack of Causal Roles of Cannabinoid and Dopamine Neurotransmitter Systems in Orbitofrontal and Piriform Cortex in Fentanyl Relapse in Rats
Claypool, S. M., Behdin, S., Applebey, S. V., Orihuel, J., Ma, Z., & Reiner, D. J. (2022) · eNeuro · doi:10.1523/eneuro.0496-21.2022 · Cited by 4 · see citing works
An interaction between basolateral amygdala orexinergic and endocannabinoid systems in inducing anti-nociception in the rat formalin test
Deli, S. B., Bonab, S. I., Khakpay, R., Khakpai, F., & Feyzi, M. H. (2022) · Psychopharmacology · doi:10.1007/s00213-022-06199-1 · Cited by 3 · see citing works
An Emergent Discriminative Learning Is Elicited During Multifrequency Testing
Zhang, X., Ye, X., Cheng, R., Li, Q., & Xiao, Z. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.01244 · Cited by 3 · see citing works
The Endocannabinoid System in the Control of Behavior
Gómez, E. S., Metna‐Laurent, M., Bellocchio, L., Busquets-García, A., & Marsicano, G. (2017) · Wiley eBooks · doi:10.1002/9781118540770.ch13 · Cited by 3 · see citing works
Local activation of CB1 receptors by synthetic and endogenous cannabinoids dampens burst firing mode of reticular thalamic nucleus neurons in rats under ketamine anesthesia
Aguirre-Rodríguez, C. A., Delgado, A., Alatorre, A., Oviedo-Chávez, A., Martínez-Escudero, J. R., Barrientos, R., & Querejeta, E. (2024) · Experimental Brain Research · doi:10.1007/s00221-024-06889-6 · Cited by 2 · see citing works
In vivo Bidirectional Modulation of Cannabinoid on the Activity of Globus Pallidus in Rats
Yu, J., Xue, Y., Wang, Y., Liu, C., & Chen, L. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2021.06.012 · Cited by 2 · see citing works
Cannabinoid Control of Fear Responses
Metna‐Laurent, M., Marsicano, G., & Gómez, E. S. (2015) · Springer eBooks · doi:10.1007/978-1-4939-2294-9_6 · Cited by 1 · see citing works
Investigating the role of the endogenous cannabinoid system in emotional modulation of pain: neurochemical and molecular mechanisms
Olango, W. M. (2012) · Arrow@dit (Dublin Institute of Technology) · doi:10.13025/17506 · Cited by 1 · see citing works
Dopamine Modulation of Emotional Learning in the Medial Prefrontal Cortex
Lauzon, N. M. (2013) · Scholarship@Western (Western University)
Self-citation
Cortical Cannabinoid Modulation of Subcortical Dopamine Activity: Implications for Emotional Processing
Draycott, B. (2013) · Scholarship@Western (Western University)
Effect of Ginsenoside Rg3 on COX-2 Expression in Brain Tissue of Lipopolysaccharide-Treated Mice
Choi, W., Cho, Y.-D., Lee, J., Shin, J.-W., Kim, S.-J., & Sohn, N. (2012) · The Korea Journal of Herbology · doi:10.6116/kjh.2012.27.6.131
Endocannabinoid Modulation of Memory for Emotionally Arousing Experiences
Morena, M., Mariani, F., Papagianni, E., & Campolongo, P. (2015) · Springer eBooks · doi:10.1007/978-1-4939-2294-9_1
Cannabinoid Transmission in the Basolateral Amygdala Modulates Prefrontal Cortex and Ventral Hippocampal Activity
Pereira, B. J. G. (2018) · Scholarship@Western (Western University)
Psychotropic Effects of Cannabis Components on the Mesolimbic Dopaminergic System
Norris, C. (2018) · Scholarship@Western (Western University)
The bidirectional effect of prelimbic 5-hydroxytryptamine type-4 (5-HT4) receptors on ACPA-mediated aversive memory impairment in adult male Sprague-Dawley rats.
Ahmadi-Mahmoodabadi, N., Emamghoreishi, M., Nasehi, M., & Zarrindast, M. (2021) · Europe PMC (PubMed Central) · doi:10.22038/ijbms.2021.49501.11317
How adolescent cannabinoid exposure sets the stage for long-term emotional and cognitive dysregulation: Impacts on molecular and neuronal risk pathways
Laviolette, S. R. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-823490-7.00001-0
Self-citation
Role of hippocampal CB1 and CB2 receptors in fear memory consolidation, extinction, and reconsolidation
Raymundi, A. M., & Stern, C. A. J. (2023) · Elsevier eBooks · doi:10.1016/b978-0-323-90877-1.00037-1
Neurological Effects of Cannabis
Ross, I. A. (2023) · Springer eBooks · doi:10.1007/978-3-031-35155-6_5
The amygdala and fear memory
Lamprecht, R. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-15754-7.00072-9
The complex interplay between stress and the endocannabinoid system in the modulation of memory function
Mancini, G. F., Morena, M., & Campolongo, P. (2025) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-443-13908-6.00020-7
Cannabinoid Control of Fear Responses
Landgraf, N. F., Sangroniz-Beltrán, L., Ceprián, M., Reyes-Velásquez, P. A., Huguet, J. E., & Gómez, E. S. (2026) · Springer eBooks · doi:10.1007/978-3-032-12239-1_6
Involvement of the cannabinoid receptors of the basolateral amygdala in the orexin A-mediated modulation of the stress-induced analgesia
aghaei, M., Khakpay, R., Khakpai, F., & Feizi, M. H. (2026) · Neuropharmacology · doi:10.1016/j.neuropharm.2026.111126

Integrated cannabinoid CB1 receptor transmission within the amygdala-prefrontal cortical pathway modulates neuronal plasticity and emotional memory encoding. Cereb Cortex (2010
Tan, H., Lauzon, N. M., Bishop, S. F., Bechard, M. A., & Laviolette, S. R. (2016)
Self-citation
Integrated cannabinoid CB1 receptor transmission within the amygdala–prefrontal cortical pathway modulates neuronal plasticity and emotional memory encoding
Tan, H., Lauzon, N. M., Bishop, S. F., Bechard, M. A., & Laviolette, S. R. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhp210 · Cited by 81 · see citing works
Self-citation
Cerebral Cortex doi:10.1093/cercor/bhp210 Integrated Cannabinoid CB1 Receptor Transmission within the Amygdala-- Prefrontal Cortical Pathway Modulates Neuronal Plasticity and Emotional Memory Encoding
Tan, H., Lauzon, N. M., Bishop, S. F., Bechard, M. A., & Laviolette, S. R. (2016)
Self-citation
Cannabinoid Transmission in the Prefrontal Cortex Bi-Phasically Controls Emotional Memory Formation via Functional Interactions with the Ventral Tegmental Area
Draycott, B., Loureiro, M., Ahmad, T., Tan, H., Zunder, J. S., & Laviolette, S. R. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1297-14.2014 · Cited by 63 · see citing works
Self-citation
Involvement of cannabinoid receptors in the amygdala and prefrontal cortex of rats in fear learning, consolidation, retrieval and extinction
Kuhnert, S., Meyer, C., & Koch, M. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.05.002 · Cited by 67 · see citing works

Authors: Tan, H., Lauzon, N. M., Bishop, S. F., Chi, N., Bechard, M., & Laviolette, S. R.
Affiliations: Western University (CA)
Natural Sciences and Engineering Research Council of Canada (CA)
Corresponding author: Laviolette, Steven R.
ORCID: Tan, Huibing
Bechard, Melanie
Laviolette, Steven R.
Venue: The Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2011-04-06
Volume: 31
Issue: 14
Pages: 5300-5312
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.4718-10.2011
PMC: PMC6622725
OpenAlex: W2054853121
Cited by: 92
References: 30
Citations by year: 2026: 2 · 2025: 2 · 2024: 3 · 2023: 5 · 2022: 5 · 2021: 6 · 2020: 7 · 2019: 3 · 2018: 7 · 2017: 5 · 2016: 8 · 2015: 10 · 2014: 13 · 2013: 6 · 2012: 7
FWCI: 6.79
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-sa
creativecommons.org/licenses/by-nc-sa/4.0/ (vor, 183 d)
Locations: Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Pharmacology › Cannabis and Cannabinoid Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: CB1 receptor, basolateral amygdala, prelimbic cortex, medial prefrontal cortex, olfactory fear conditioning, emotional salience, neuronal firing rate, burst firing, single-unit electrophysiology
MeSH terms: Action Potentials, Afferent Pathways, Amygdala, Analysis of Variance, Animals, Arachidonic Acids, Calcium Channel Blockers, Cannabinoids, Dose-Response Relationship, Drug, Electroshock, Fear, Functional Laterality, Male, Memory, Morpholines, Naphthalenes, Neural Inhibition, Neurons, Piperidines, Pyrazoles, Smell, Rats, Sprague-Dawley, Prefrontal Cortex, Receptor, Cannabinoid, CB1, Benzoxazines, 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

Cannabinoid transmission in the basolateral amygdala modulates fear memory formation via functional inputs to the prelimbic cortex

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks