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Busquets-Garcia, A. Differential role of anandamide and 2-arachidonoylglycerol in memory and anxiety-like responses. Psychiatry 70 , — This study shows that anxiolytic-like effects of AEA are mediated by CB1R and associated with memory disruption, whereas 2-AG induces an anxiolytic effect via CB2R without affecting cognitive functions. Kinsey, S.

Inhibition of endocannabinoid catabolic enzymes elicits anxiolytic-like effects in the marble burying assay. Sciolino, N. Enhancement of endocannabinoid signaling with JZL, an inhibitor of the 2-arachidonoylglycerol hydrolyzing enzyme monoacylglycerol lipase, produces anxiolytic effects under conditions of high environmental aversiveness in rats. Zhong, P. Monoacylglycerol lipase inhibition blocks chronic stress-induced depressive-like behaviors via activation of mTOR signaling. Neuropsychopharmacology 39 , — Marsch, R. Reduced anxiety, conditioned fear, and hippocampal long-term potentiation in transient receptor potential vanilloid type 1 receptor-deficient mice.

Sun, F. Increased expression of TRPV1 in the cortex and hippocampus from patients with mesial temporal lobe epilepsy. The transient receptor potential vanilloid-1 is localized at excitatory synapses in the mouse dentate gyrus. Brain Struct. Chavez, A. TRPV1 activation by endogenous anandamide triggers postsynaptic long-term depression in dentate gyrus. Bahi, A. Targeting the endocannabinoid system in the treatment of fragile X syndrome. Aguiar, D. Anxiolytic-like effects induced by blockade of transient receptor potential vanilloid type 1 TRPV1 channels in the medial prefrontal cortex of rats.

Psychopharmacology Berl. Almeida-Santos, A.

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Modulation of anxiety-like behavior by the endocannabinoid 2-arachidonoylglycerol 2-AG in the dorsolateral periaqueductal gray. Brain Res. Terzian, A. Modulation of anxiety-like behaviour by transient receptor potential vanilloid type 1 TRPV1 channels located in the dorsolateral periaqueductal gray. Cannabinoid type 1 receptors and transient receptor potential vanilloid type 1 channels in fear and anxiety-two sides of one coin?

LeDoux, J. Emotion circuits in the brain. Pape, H. Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear. Nader, K. A single standard for memory: the case for reconsolidation. Myers, K.

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Mechanisms of fear extinction. Psychiatry 12 , — Maren, S. Seeking a spotless mind: extinction, deconsolidation, and erasure of fear memory. Neuron 70 , — The endogenous cannabinoid system controls extinction of aversive memories. This was the first study to demonstrate the effect of the eCB system on acquired fear response. Plendl, W.

Dissociation of within- and between-session extinction of conditioned fear. Dubreucq, S. Genetic dissection of the role of cannabinoid type-1 receptors in the emotional consequences of repeated social stress in mice. Llorente-Berzal, A. Trouche, S. Fear extinction causes target-specific remodeling of perisomatic inhibitory synapses. Neuron 80 , — Bowers, M. Interaction between the cholecystokinin and endogenous cannabinoid systems in cued fear expression and extinction retention.

Soria-Gomez, E. Habenular CB receptors control the expression of aversive memories. Neuron 88 , — Pan, B. Blockade of 2-arachidonoylglycerol hydrolysis by selective monoacylglycerol lipase inhibitor 4-nitrophenyl 4- dibenzo[ d ][1,3]dioxolyl hydroxy methyl piperidinecarboxylate JZL enhances retrograde endocannabinoid signaling. Alterations of endocannabinoid signaling, synaptic plasticity, learning, and memory in monoacylglycerol lipase knock-out mice.

Lin, H. The role of prefrontal cortex CB 1 receptors in the modulation of fear memory. Cortex 19 , — Convergent translational evidence of a role for anandamide in amygdala-mediated fear extinction, threat processing and stress-reactivity. Psychiatry 18 , — This study provides evidence for the conserved role of AEA in rodents and humans regarding amygdala function and threat processing. Kandel, E. The molecular biology of memory storage: a dialogue between genes and synapses. Science , — Cannabinoid CB 1 receptor mediates fear extinction via habituation-like processes.

Endocannabinoids mediate acute fear adaptation via glutamatergic neurons independently of corticotropin-releasing hormone signaling. Inhibition of restraint stress-induced neural and behavioural activation by endogenous cannabinoid signalling. Ganon-Elazar, E. Cannabinoid receptor activation in the basolateral amygdala blocks the effects of stress on the conditioning and extinction of inhibitory avoidance. Cannabinoids and traumatic stress modulation of contextual fear extinction and GR expression in the amygdala-hippocampal-prefrontal circuit.

Psychoneuroendocrinology 38 , — Laricchiuta, D. Effects of endocannabinoid and endovanilloid systems on aversive memory extinction. Gozzi, A. A neural switch for active and passive fear. Neuron 67 , — Koolhaas, J. Neuroendocrinology of coping styles: towards understanding the biology of individual variation. Bimodal control of fear-coping strategies by CB 1 cannabinoid receptors. Suppression of amygdalar endocannabinoid signaling by stress contributes to activation of the hypothalamic—pituitary—adrenal axis.

Neuropsychopharmacology 34 , — Gray, J. Corticotropin-releasing hormone drives anandamide hydrolysis in the amygdala to promote anxiety. Endocrinology , — Recruitment of prefrontal cortical endocannabinoid signaling by glucocorticoids contributes to termination of the stress response. Evanson, N. Fast feedback inhibition of the HPA axis by glucocorticoids is mediated by endocannabinoid signaling.

Glangetas, C. Crosby, K. Endocannabinoids gate state-dependent plasticity of synaptic inhibition in feeding circuits. Neuron 71 , — Downregulation of endocannabinoid signaling in the hippocampus following chronic unpredictable stress. Neuropsychopharmacology 30 , — This study provides strong evidence that the eCB system is dysregulated under chronic stress. Rossi, S. Chronic psychoemotional stress impairs cannabinoid-receptor-mediated control of GABA transmission in the striatum. Wang, W. Deficiency in endocannabinoid signaling in the nucleus accumbens induced by chronic unpredictable stress.

Neuropsychopharmacology 35 , — Hillard, C. Di Marzo, V. Haj-Dahmane, S. Chronic stress impairs alpha1-adrenoceptor-induced endocannabinoid-dependent synaptic plasticity in the dorsal raphe nucleus. Disruption of fatty acid amide hydrolase activity prevents the effects of chronic stress on anxiety and amygdalar microstructure.

Wamsteeker, J. Repeated stress impairs endocannabinoid signaling in the paraventricular nucleus of the hypothalamus. This paper demonstrates the mechanistic underpinnings for how repeated stress interferes with eCB system activity. Cannabinoid CB 1 receptor in the modulation of stress coping behavior in mice: the role of serotonin and different forebrain neuronal subpopulations.

Neuropharmacology 65 , 83—89 Steiner, M. Conditional cannabinoid receptor type 1 mutants reveal neuron subpopulation-specific effects on behavioral and neuroendocrine stress responses. Psychoneuroendocrinology 33 , — Repeated homotypic stress elevates 2-arachidonoylglycerol levels and enhances short-term endocannabinoid signaling at inhibitory synapses in basolateral amygdala.

Russo, S. Neurobiology of resilience. Franklin, T. Neural mechanisms of stress resilience and vulnerability. Neuron 75 , — Tye, K. Optogenetic investigation of neural circuits underlying brain disease in animal models. Masseck, O. The endocannabinoid system controls food intake via olfactory processes.

Quarta, C. CB1 signaling in forebrain and sympathetic neurons is a key determinant of endocannabinoid actions on energy balance. Bellocchio, L. Activation of the sympathetic nervous system mediates hypophagic and anxiety-like effects of CB1 receptor blockade. USA , — Araque, A. Gliotransmitters travel in time and space. Belanger, M. Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Walter, L. ATP induces a rapid and pronounced increase in 2-arachidonoylglycerol production by astrocytes, a response limited by monoacylglycerol lipase. Cannabinoid and cannabinoid-like receptors in microglia, astrocytes, and astrocytomas.

Glia 58 , — Endocannabinoids potentiate synaptic transmission through stimulation of astrocytes. Neuron 68 , — Min, R. Astrocyte signaling controls spike timing-dependent depression at neocortical synapses. Gomez-Gonzalo, M. Endocannabinoids induce lateral long-term potentiation of transmitter release by stimulation of gliotransmission. Cortex 25 , — Ostroff, L. Synapses lacking astrocyte appear in the amygdala during consolidation of Pavlovian threat conditioning.

Hagemann, T. Deficits in adult neurogenesis, contextual fear conditioning, and spatial learning in a Gfap mutant mouse model of Alexander disease. Clark, D. Suzuki, A. Astrocyte-neuron lactate transport is required for long-term memory formation. The most representative form is the Pfizer compound CP , a potent and complete agonist at both the CB 1 and CB 2 receptors, which was used to characterize the CB 1 receptor for the first time Devane et al. Aminoalkylindoles were the first non-cannabinoid molecules that displayed cannabimimetic activity Pacheco et al. Eicosanoids are the prototypic endocannabinoids Fig.

Cannabinoid receptor antagonists. Several series of compounds have been developed as CB 1 receptor antagonists. The most representative are diarylpyrazoles, substituted benzofuranes, aminoalkylindoles and triazole derivatives. They were synthesized by Sanofi and are considered the reference antagonists. However, they are not neutral antagonists since they display significant inverse agonist properties.

Diarylpyrazoles are orally active and are currently under clinical trials for the treatment of obesity. Substituted benzofuranes include LY , a CB 1 receptor antagonist with affinity at serotonin and muscarinic receptors Felder et al. Aminoalkylindoles include a CB 2 receptor antagonist, AM , which also displays activity as a low-affinity partial CB 1 agonist Howlett et al. Triazole derivatives include LH Jagerovic et al.

Uptake blockers. Based on the structure of anandamide, a series of eicosanoid derivatives that have the ability to block anandamide transport have been synthesized. The molecular structures of the three prototypical uptake blockers are depicted in Fig. The first and best studied transport inhibitor is AM Beltramo et al. The administration of AM results in the accumulation of anandamide and potentiates the effects of exogenously administered anandamide. Structure of three anandamide uptake blockers. UCM is the compound with the highest affinity at the anandamide transporter.

AM was the first blocker designed and has been extensively described. Both molecules, however, had a significant impact on the activity of the fatty acid amidohydrolase FAAH , the enzyme that degrades anandamide. AM is a recently described compound without inhibitory action at FAAH, which has been used to demonstrate the independence of anandamide transport and degradation processes. Inhibitors of fatty acid amide hydrolase. As in the case of the cannabinoid receptors, different lines of research have led to the discovery of chemically heterogeneous FAAH inhibitors.

The earlier inhibitors described consisted of reversible electrophilic carbonyl inhibitors trifluoromethyl ketones, alpha-keto esters and amides, and aldehydes or irreversible inhibitors sulfonyl fluorides and fluorophosphonates incorporated into the fatty acid structures.

Based on the structure of alpha-trifluoromethyl ketones a series of potent inhibitors were developed. Of these, alpha-keto N 4 -oxazolopyridine provides inhibitors that are 10 2 —10 3 times more potent than the corresponding trifluoromethyl ketones Boger et al. A recent series of alpha heterocycles has been shown to possess very high potency and selectivity to reversibly inhibit FAAH activity in vivo and in vitro.

The most potent of these new compounds is OL, which exhibits IC50 in the low nanomolar range Lichtman et al. A different strategy has been selected by the group of Piomelli et al. These new classes of inhibitors are carbamate derivatives capable of directly interacting with the serine nucleophile of FAAH. However, these new inhibitors, although extremely potent, are not selective because they may potentially inactivate other serine hydrolases such as heart triacylglycerol hydrolase Lichtman et al.

The ubiquitous presence of the endogenous cannabinoid system correlates with its role as a modulator of multiple physiological processes. A comprehensive analysis of all the functions of the endocannabinoids is beyond the scope of the present review. The reader will find an extensive list of recent reviews that explore the physiological relevance of the endogenous cannabinoid system, as depicted in Table 1.

In this section, we focus on the cellular and system physiological events mediated by endocannabinoids that are relevant to our understanding of the contribution of the endogenous cannabinoid system in alcoholism. Cellular physiology. As described in the section on biochemistry of the endogenous cannabinoid system, endocannabinoids are released upon demand after cellular depolarization or receptor stimulation in a calcium-dependent manner.

Once produced, they act on the cannabinoid receptors located in the cells surrounding the site of production. This property indicates that endocannabinoids are local mediators similar to the autacoids e. In the CNS, the highly organized distribution of endocannabinoid signalling elements in GABAergic and glutamatergic synapses and their preservation throughout evolution suggests a pivotal role in synaptic transmission. If endocannabinoids act postsynaptically they will counteract the activatory inputs entering the postsynaptic cells. This mechanism has been proposed for postsynaptic interactions with dopaminergic transmission Felder et al.

Despite its importance, this effect is secondary to the important presynaptic actions whose existence is supported by two facts: i the concentration of the CB 1 receptors in presynaptic terminals and ii the well-documented inhibitory effects of the CB 1 receptor agonists on the release of GABA, glutamate, acetylcholine and noradrenaline Schlicker and Kathmann, ; Piomelli, Presynaptic inhibition of transmitter release by endocannabinoids may adopt two different forms of short-term synaptic plasticity, depending on the involvement of GABA or glutamate transmission, respectively: depolarization-induced suppression of inhibition DSI and depolarization-induced suppression of excitation DSE Wilson and Nicoll, ; Diana and Marty, Both forms of synaptic plasticity involve the initial activation of a postsynaptic large projecting neuron pyramidal or Purkinje cells that sends a retrograde messenger to a presynaptic GABA terminal DSI or a presynaptic glutamate terminal DSE , inducing a transient suppression of either the presynaptic inhibitory or the presynaptic excitatory input.

The contribution of endocannabinoids to these forms of short-term synaptic plasticity has been described in the hippocampus Wilson and Nicoll, ; Wilson et al. The nature of the endocannabinoid system acting as a retrograde messenger is still unknown. The role of endocannabinoid-induced DSI or DSE seems to be the coordination of neural networks within the hippocampus and the cerebellum that are involved in relevant physiological processes, such as memory or motor coordination.

Additional forms of endocannabinoid modulation of synaptic transmission involve the induction of long-term synaptic plasticity, namely long-term potentiation LTP and long-term depression LTD. Both forms of synaptic plasticity involve long-term changes in the efficacy of synaptic transmission in glutamatergic neurons, which have a major impact on consolidation and remodelling of the synapsis. Activation of the cannabinoid receptors prevents the induction of LTP in the hippocampal synapses Stella et al. Overall, endocannabinoids act as local messengers that adjust synaptic weight and contribute significantly to the elimination of information flow through specific synapses in a wide range of time frames.

The fact that cannabinoid receptor stimulation has a major impact on second messengers involved not only in synaptic remodelling Derkinderen et al. Both processes are relevant for homeostatic behaviour such as motivated behaviour feeding, reproduction, relaxation, sleep and emotions, as well as for cognition, since learning and memory require dynamic functional and morphologic changes in brain circuits.

An experimental confirmation of this hypothetical role of the endogenous cannabinoid system was the demonstration of its role in the control of the extinction of aversive memories Marsicano et al. System physiology. The cellular effects of endogenous cannabinoids have a profound impact on the main physiological systems that control body functions Table 1. Despite the peripheral modulation of the immune system, vascular beds, reproductive organs, gastrointestinal motility and metabolism, the endogenous cannabinoid system tightly regulates perception processes including nociception cannabinoids are potent analgetics, Martin and Litchman, and visual processing in the retina Straiker et al.

Additional functions exerted by the endogenous cannabinoid system involve the regulation of basal ganglia and cerebellar circuits, where it is involved in the modulation of implicit learning of motor routines Rodriguez de Fonseca et al. Among the varied functions in which the endogenous cannabinoid system is engaged, the homeostatic control of emotions and the regulation of motivated behaviour merit special attention because of its impact on human diseases, including addiction.

The endogenous cannabinoid system controls the motivation for appetite stimuli, including food and drugs Di Marzo et al. The positive effects of endocannabinoids on motivation seem to be mediated not only by the peripheral sensory systems in which cannabinoid receptors are present i. The endogenous cannabinoid system is widely distributed in the extended amygdala, a set of telencephalic nuclei located in medial septal neurons, the nucleus accumbens shell and amygdalar complex, and are involved in the control of motivated behaviour, conditioned responses and gating-associated emotional responses.

This hypothesis is supported by two facts: the inhibition of motivated behaviour observed after administration of a cannabinoid antagonist Colombo et al. Research on the neurobiological basis of endocannabinoid effects on motivated behaviour has focused on endocannabinoid—dopamine interaction as well as on the role of the endocannabinoid system in habit learning and conditioning.

Most drugs of dependence activate the VTA dopaminergic neurons, as monitored by the dopamine release in terminal areas, especially in the nucleus accumbens and prefrontal cortex, or by the firing rates of VTA dopaminergic neurons. THC and other CB 1 receptor agonists increase dopamine efflux in the nucleus accumbens and prefrontal cortex and increase the dopaminergic cell firing in the VTA for review see Gardner and Vorel, This effect is not caused by the direct activation of dopaminergic neurons because they do not express CB 1 receptors Julian et al.

Although the effects of cannabinoid agonists on dopamine release in the projecting areas i. This discrepancy may suggest the existence of a differential role for endogenous opioid systems as the modulators of cannabinoid actions in dopamine cell bodies with respect to their axon terminals. In agreement with these actions of cannabinoids in brain reward circuits, repeated cannabinoid exposure can induce behavioural sensitization similar to that produced by other drugs of dependence.

Interestingly, administration of a CB 1 receptor antagonist blocks cue-induced reinstatement to heroin and cocaine self-administration De Vries et al. The importance of the endogenous cannabinoid system in the control of motivated behaviour goes far beyond the control of processing ongoing reward signals. The CB 1 receptors are apparently involved in the control of reward homeostasis Sanchis-Segura et al.

Moreover, when cannabinoid homeostatic mechanisms are not adequate to restore the lost equilibrium in reward control derived from continuous uncontrolled exposure to a reinforcer e. This has been demonstrated in rodents exposed to cycles of dependence—abstinence to alcohol and morphine Navarro et al. Whether these allostatic changes occur in other models of motivated behaviour i.

Cannabinoid receptors are not only associated with motivational disturbances, but also related to emotional processing. A key station for the endocannabinoid regulation of emotions is the amygdalar complex. The final balance will lead to anxiety or anxiolysis, depending on the rate of activation of descending projections of the central nucleus of the amygdala to the hypothalamus endocrine responses and brain stem behavioural and autonomic responses.

However, recent studies indicate that anxiolysis is the normal response to enhanced cannabinoid transmission in the limbic system, as reflected by the phenotype of FAAH knockout mice and the effects of FAAH inhibitors Cravatt et al. The induction of anxiety by cannabinoid receptor antagonists Navarro et al.

The presence of the endogenous cannabinoid system in reward circuits and its role in motivational and emotional homeostasis suggests that drugs which modulate cannabinoid signalling might serve as therapeutic tools in drug addiction. In accordance with this rationale, the CB 1 receptor antagonists are able to modulate opioid self-administration in rodents Navarro et al.

Extending this hypothesis, converging research lines have established a role for both anandamide and the CB 1 receptor in alcohol dependence Hungund and Basaravajappa, ; Hungund et al. The administration of CB 1 receptor agonists promotes alcohol intake Colombo et al. Molecular studies have shown that chronic alcohol administration is associated with an increased formation of both anandamide and its membrane precursor NAPE Basavarajappa and Hungund, Chronic alcohol exposure also resulted in the stimulation of a second endocannabinoid, 2-AG Basavarajappa et al.

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Animal studies also revealed that chronic exposure to alcohol downregulated the CB 1 receptors in the brain Basavarajappa et al. Finally, a recent gene screening study has identified the CB 1 receptor as one of the genes whose expression is permanently affected by serial cycles of alcohol dependence and withdrawal Rimondini et al. These data indicate a role for the endogenous cannabinoid system as a relevant contributor to alcoholism. In the present issue, the reader will find additional experimental approaches to the role of the endogenous cannabinoid system in alcoholism.

Since the discovery of anandamide, the increasing information on the physiological roles played by the endogenous cannabinoid system and its contribution to pathology have led to this signalling system becoming more important in neurobiology. The intense pharmacological research based on this information has yielded, in a very short time, potent, selective drugs targeting the endogenous cannabinoid system that have opened up new avenues for the understanding and treatment of major diseases including cancer, pain, neurodegeneration, anxiety and addiction. This is a very promising starting point for a new age that takes over from the ancient use of Cannabis as a medicine.

Now is the time for clinical trials aimed at evaluating the efficacy of cannabinoid drugs in disorders lacking effective therapeutic approaches, such as alcoholism. Oxford University Press is a department of the University of Oxford. It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide. Sign In or Create an Account. Sign In. Advanced Search. Article Navigation. Close mobile search navigation Article Navigation. Volume Article Contents.

Oxford Academic. Google Scholar. Cite Citation. Permissions Icon Permissions. Abstract The endogenous cannabinoid system is an ubiquitous lipid signalling system that appeared early in evolution and which has important regulatory functions throughout the body in all vertebrates. Table 1. Open in new tab. Open in new tab Download slide. Table 2. Basavarajappa, B. Batkai, S. Beltramo, M. Beinfeld, M. Bisogno, T. Boger, D. Pape, B. Ventral tegmental area cannabinoid type-1 receptors control voluntary exercise performance..

Bellocchio, E. Soria-Gomez, C. Quarta, M. Metna-Laurent, P. Cardinal, E. Binder, A. Cannich, A. Delamarre, M. Haring, M. Martin-Fontecha, D. Vega, T. Leste-Lasserre, D. Bartsch, K. Monory, B. Lutz, F. Chaouloff, U. Pagotto, M. Guzman, D. Cota, G. Proceedings of the National Academy of Sciences. Neuron-type specific cannabinoid-mediated G protein signalling in mouse hippocampus.. Two-photon excitation STED microscopy in two colors in acute brain slices.. Biophysical Journal. Striatal GABAergic and cortical glutamatergic neurons mediate contrasting effects of cannabinoids on cortical network synchrony..

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Soria-Gomez, G. Buzsaki, G. Marsicano, D. Anti-inflammatory lipoxin A4 is an endogenous allosteric enhancer of CB1 cannabinoid receptor..

Behavioral Neurobiology of the Endocannabinoid System

Pamplona, J. Ferreira, O. Menezes de Lima, F. Duarte, A. Bento, S. Forner, J. Villarinho, L. Bellocchio, C. Wotjak, R. Lerner, K. Lutz, C. Canetti, I. Matias, J.

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Calixto, G. Guimaraes, R. Hypothalamic CB1 cannabinoid receptors regulate energy balance in mice.. Endocannabinoids measurement in human saliva as potential biomarker of obesity.. Cannabinoid CB1 receptor deficiency increases contextual fear memory under highly aversive conditions and long-term potentiation in vivo.. Neurobiology of Learning and Memory. Metna-Laurent, E. Soria-Gomez, D. Verrier, M. Conforzi, P. Jego, P. Lafenetre, G. Genetic dissection of the role of cannabinoid type-1 receptors in the emotional consequences of repeated social stress in mice.. Cannabinoid type 1 receptors located on single-minded 1-expressing neurons control emotional behaviors..

Dubreucq, S. Kambire, M. Conforzi, M. Metna-Laurent, A. Cannich, E. Soria-Gomez, E. Richard, G. Acute cannabinoids impair working memory through astroglial CB1 receptor modulation of hippocampal LTD.. Developmental regulation of CB1-mediated spike-time dependent depression at immature mossy fiber-CA3 synapses. Maddalena D. Giovanni Marsicano, Francis Chaouloff. State-dependent, bidirectional modulation of neural network activity by endocannabinoids..

Piet, A. Garenne, F. Farrugia, G. Le Masson, G. Marsicano, P. Chavis, O. GABAergic and cortical and subcortical glutamatergic axon terminals contain CB1 cannabinoid receptors in the ventromedial nucleus of the hypothalamus.. Simultaneous postprandial deregulation of the orexigenic endocannabinoid anandamide and the anorexigenic peptide YY in obesity.. Daniela Cota, Giovanni Marsicano. European Journal of Neuroscience. Endocannabinoids and motor behavior: CB1 receptors also control running activity.. Emotional consequences of wheel running in mice: which is the appropriate control?. Presynaptic CB1 receptors regulate synaptic plasticity at cerebellar parallel fiber synapses..

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Journal of Neurophysiology. Lucas, Justo G. CB1 receptor deficiency decreases wheel-running activity: consequences on emotional behaviours and hippocampal neurogenesis.. Abrous, Giovanni Marsicano, Francis Chaouloff. Experimental Neurology. CB 1 signaling in forebrain and sympathetic neurons is a key determinant of endocannabinoid actions on energy balance.. Cell Metabolism.

Bimodal control of stimulated food intake by the endocannabinoid system.. Localization and function of the cannabinoid CB1 receptor in the anterolateral bed nucleus of the stria terminalis.. Manzoni, Pedro Grandes. Bidirectional regulation of novelty-induced behavioral inhibition by the endocannabinoid system.. Self-modulation of neocortical pyramidal neurons by endocannabinoids..

Endocannabinoids render exploratory behaviour largely independent of the test aversiveness: role of glutamatergic transmission.. Jacob, A. Yassouridis, G. Marsicano, K. Genes, Brain and Behavior. Spinal endocannabinoids and CB1 receptors mediate C-fiber-induced heterosynaptic pain sensitization.. Pernia-Andrade, A. Kato, R. Witschi, R. Nyilas, I. Katona, T. Freund, M. Watanabe, J. Filitz, W. Koppert, J. Schuttler, G. Ji, V. Neugebauer, G. Marsicano, B. Lutz, H. Vanegas, H. Cannabinoid modulation of hippocampal long-term memory is mediated by mTOR signaling..

David A. Price, Alex A. Roberts, Andrea Giuffrida. Endocannabinoids mediate acute fear adaptation via glutamatergic neurons independently of corticotropin-releasing hormone signaling.. Kamprath, W. Plendl, G. Marsicano, J. Deussing, W. Wurst, B. Roles of the endocannabinoid system in learning and memory.. Behavioral Neurobiology of the Endocannabinoid System.

Hepatic CB1 receptor is required for development of diet-induced steatosis, dyslipidemia, and insulin and leptin resistance in mice.. Conditional cannabinoid receptor type 1 mutants reveal neuron subpopulation-specific effects on behavioral and neuroendocrine stress responses..

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