Aversive memory and the role of the mesocorticolimbic system in defensive responses-literature review
DOI:
https://doi.org/10.36560/1242019871Palavras-chave:
Memory, Emotion, Fear, Limbic System, Mesencephalon, Prefrontal cortex, DopamineResumo
Evidence from both animal and human research indicates that emotionally significant experiences activate hormonal and brain systems that regulate the consolidation of new memories. Mesocorticolimbic dopamine system has been shown to be critical for many processes that drive learning and memory, including motivation, prediction error, incentive salience, memory consolidation, and response output; and it carries signals of valorization, both for stimuli related to gain, and for aversive stimuli. Literature indicates that dopaminergic system is involved in fear conditioning and extinction. Emotional processes are mainly mediated by the amygdala, and when it becomes active, its anatomical connections with the cortex may facilitate the processing of the presented stimuli. The ventral tegmental area encodes the prediction of errors, and signals are transmitted to regions such as nucleus accumbens, amygdala, hippocampus and prefrontal cortex. Advances in neurobiological research favored the understanding of the mechanisms underlying learning and the evocation of the extinction of aversive memory. We review the behavioral and neurobiological literature showing a role for mesocorticolimbic structures in defensive responses and aversive memory.
Â
Â
Referências
ABRAHAM, A.D.; NEVE, K.A.; LATTAL, K.M. Dopamine and extinction: A convergence of theory with fear and reward circuitry. Neurobiol Learn Mem, v.0, p.65–77, 2014.
ABRAHAM, A.D.; NEVE, K.A.; LATTAL, K.M. Activation of D1/5 dopamine receptors: a common mechanism for enhancing extinction of fear and reward-seeking behaviors. Neuropsychopharmacology. 2016a, vol.41, n.8, p.2072-81.
ABRAHAM, A.D.; NEVE, K.A.; LATTAL, K.M. Effects of D1 receptor knockout on fear and reward learning. Neurobiol Learn Mem, 2016b, vol.133, p.265-73,
ADMON, R.; MILAD, M.R.; HENDLER, T. A causal model of post-traumatic stress disorder: disentangling predisposed from acquired neural abnormalities. Trends in Cognitive Sciences, 2013, vol.17, n.7, p.337-347.
Badrinarayan, A.; Wescott, S.A.; Weele, C.M.V; Saunders, B.T.; Couturier, B.E.; Maren, S.; Aragona, B.J. Aversive stimuli differentially modulate real-time dopamine transmission dynamics within the nucleus accumbens core and shell. J Neurosci., 2012, vol.32, n.45, p.15779–15790.
BEAULIEU, J.M.; GAINETDINOV, R.R. The physiology, signaling, and pharmacology of dopamine receptors. Pharmacol Rev., 2011, vol.63, n.1, p.182–217.
BECCHETTI, A. Hippocampal formation and the classical art of memory. PNAS, 2010, vol. 107, n.25.
BELIN, D.; JONKMAN, S.; DICKINSON, A., ROBBINS, T.W., and EVERITT, B.J. Parallel and interactive learning processes within the basal ganglia: relevance for the understanding of addiction. Behav. Brain Res., 2009, vol.199, p.89–102.
BELUJON, P.; GRACE, A.A. Regulation of dopamine system responsivity and its adaptive and pathological response to stress. Proc. R. Soc. B., 2015, vol.282, n.20142516, p.1-10.
BERLAU, D.J.; MCGAUGH, J.L. Enhancement of extinction memory consolidation: The role of the noradrenergic and GABAergic systems within the basolateral amygdala. Neurobiology of Learning and Memory, v.86, p.123–132, 2006.
BISSON, J.I.; COSGROVE, S.; LEWIS, C.; ROBERTS, N.P. Post-traumatic stress disorder. BMJ, 2015; vol.351, n.h6161.
BRISCHOUX, F. et al. Phasic excitation of dopamine neurons in ventral VTA by noxious stimuli. Proceedings of the National Academy of Sciences, v. 106, n. 12, p. 4894-4899, 2009.
Bromberg-Martin, E.S.; Matsumoto, M.; HikosakA, O. Dopamine in motivational control: rewarding, aversive, and alerting. Neuron., 2010, vol.68, n.5, p.815–834.
Buckley, C.T.; Caldwell, K.K. Fear conditioning is associated with altered integration of PLC and ERK signaling in the hippocampus. Pharmacol Biochem Behav. 2004, vol.79, n.4, p.633–640.
BUKALO, O. et al. Prefrontal inputs to the amygdala instruct fear extinction memory formation. Sci. Adv., 2015, vol.1, n.e1500251.
Busti, D.; Geracitano, R.; Whittle, N.; Dalezios, Y.; Manko, M.; Kaufmann, W.; Ferraguti, F. Different fear states engage distinct networks within the intercalated cell clusters of the amygdala. J Neurosci., 2011, vol.31, n.13, p.5131–5144.
CHAVEZ, C.M.; MCGAUGH, J.L.; WEINBERGER, N.M. Activation of the basolateral amygdala induces long-term enhancement of specific memory representations in the cerebral cortex. Neurobiology of Learning and Memory, v.101, p.8–18, 2013.
DUVARCI, S.; PARE, D. Amygdala microcircuits controlling learned fear. Neuron., 2014, vol.82, n.5, p. 966-980.
EL-GHUNDI, M.; O'DOWD, B.F.; GEORGE, S.R. Prolonged fear responses in mice lacking dopamine D1 receptor. Brain Res., 2001, vol.892, n.1, p.86-93.
ESPIRIDIÃO-ANTÔNIO, V. et al. Neurobiologia das emoções. Rev. Psiq. ClÃn. v.35, n.2, p.55-65, 2008.
ESPEJO, E.F. Prefrontocortical dopamine loss in rats delays long-term extinction of contextual conditioned fear, and reduces social interaction without affecting short-term social interaction memory. Neuropsychopharmacology., 2003, vol.28, n.3, p.490–498.
ETKIN, A.; WAGER, T.D. Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. Am J Psychiatry., 2007, vol.164, n.10, p.1476–1488.
FADOK, J.P.; DICKERSON, T.M.; PALMITER, R.D. Dopamine is necessary for cue-dependent fear conditioning. J Neurosci., 2009, vol.29, n.36, p.11089–11097.
FADOK, J.P.; DARVAS, M.; DICKERSON, T.M.; PALMITER, R.D. Long-term memory for pavlovian fear conditioning requires dopamine in the nucleus accumbens and basolateral amygdala. PLoS One., 2010, vol.5, n.9.
GILL, K.M.; GRACE, A.A. Heterogeneous processing of amygdala and hippocampal inputs in the rostral and caudal subregions of the nucleus accumbens. Int J Neuropsychopharmacol., 2011, vol.14, n.10, p.1301– 1314.
GLANNON, W. Psychopharmacology and memory. J Med Ethics. 2006, vol.32, p.74–78. doi: 10.1136/jme.2005.012575.
GOTO, Y.; OTANI, S.; GRACE, A.A. The Yin and Yang of dopamine release: a new perspective. Neuropharmacology, 2007, vol.53, p.583-587, doi:10.1016/j.neuropharm.2007.07.007.
GOULD, T.D.; MANJI, H.K. DARPP-32: A molecular switch at the nexus of reward pathway plasticity. Proc Natl Acad Sci USA., 2005, vol.102, n.2, p.253–254.
GU, Y. et al. Neural activities underlying the feedback express salience prediction errors for appetitive and aversive stimuli. Sci. Rep., 2016, vol.6, n.34032
GUARACI, F.A.; FROHARDT, R.J.; KAPP, B.S. Amygdaloid D1 dopamine receptor involvement in Pavlovian fear conditioning. Brain Res., 1999, vol.827, n.1–2, p.28–40.
HAGENA, H.; MANAHAN-VAUGHAN, D. Dopamine D1/D5, but not D2/D3, receptor dependency of synaptic plasticity at hippocampal mossy fiber synapses that is enabled by patterned afferent stimulation, or spatial learning. Frontiers in synaptic neuroscience, 2016, vol. 8.
HEATH, F.C. et al. Dopamine D1-like receptor signalling in the hippocampus and amygdala modulates the acquisition of contextual fear conditioning. Psychopharmacology (Berl)., 2015, vol.232, n.14, p.2619-29, doi: 10.1007/s00213-015-3897-y.
HEGERL, U.; SANDER, C.; HENSCH, T. Arousal regulation in affective disorders. In: FRODL, T. (Ed.). Systems Neuroscience in Depression. Elsevier San Diego, 2016, p.341-370.
HIKIND, N.; MAROUN, M. Microinfusion of the D1 receptor antagonist, SCH23390 into the IL but not the BLA impairs consolidation of extinction of auditory fear conditioning. Neurobiol Learn Mem. 2008; 90(1):217–222.
Holtzman-Assif, O.; Laurent, V.; Westbrook, R.F. Blockade of dopamine activity in the nucleus accumbens impairs learning extinction of conditioned fear. Learn Mem., 2010, vol.17, n.2, p.71–75.
HORNER, A.J.; BURGESS,N. The associative structure of memory for multi-element events. Journal of Experimental Psychology: General, 2013, vol. 142, n. 4, p.1370–1383.
HU, J.L.; LIU, G.; LI, Y.C.; GAO, W.J.; HUANG, Y.Q. Dopamine D1 receptor-mediated NMDA receptor insertion depends on Fyn but not Src kinase pathway in prefrontal cortical neurons. Mol Brain., 2010, vol.3, n.20, p.1-14.
HUGUES, S.; GARCIA, R.; LENA, I. Time course of extracellular catecholamine and glutamate levels in the rat medial prefrontal cortex during and after extinction of conditioned fear. Synapse., 2007, vol.61, n.11, p.933–937.
IKEGAMIL, M.; UEMURAL, T.; KISHIOKAL, A.; SAKIMURA, K.; MISHINA, M. Striatal dopamine D1 receptor is essential for contextual fear conditioning. Nature/Scientific Reports, 2014, vol.4, n.3976, p.1-10.
KANDEL, E.R. et al. PrincÃpios de neurociências. 5.ed. Porto Alegre: AMGH, 2014.
KANDEL, E.R.; SCHWARTZ, J.H.; JESSEL, T.M. Fundamentos da neurociência e do comportamento. Rio de Janeiro: Guanabara Koogan, 2000.
KRISHNA, A.; STRACK, F. Reflection and impulse as determinants of human behavior. In: MEUSBURGER, P.; WERLEN, B.; SUASANA, L. (eds.). Knowledge and Action. Knowledge and Space, vol.9, Springer Open, 2017.
LaLumiere, R.T.; Nawar, E.M.; McGaugh, J.L. Modulation of memory consolidation by the basolateral amygdala or nucleus accumbens shell requires concurrent dopamine receptor activation in both brain regions. Learn Mem., 2005, vol.12, n.3, p.296–301.
Lammel, S.; Ion, D.I.; Roeper, J.; Malenka, R.C. Projection-specific modulation of dopamine neuron synapses by aversive and rewarding stimuli. Neuron., 2011, vol.70, n.5, p.855–862.
LANG, S.; KROLL, A.; LIPINSKI, S.J.; WESSA, M.; RIDDER, S.; CHRISTMANN, C.; SCHAD, L.R.; FLOR, H. Context conditioning and extinction in humans: differential contribution of the hippocampus, amygdala and prefrontal cortex. European Journal of Neuroscience, 2009, vol. 29, p. 823–832.
LAUZON, N.M.; BECHARD, M.; AHMAD, T.; LAVIOLETTE, S.R. 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. Neuropharmacology. 2013; vol.67, p.104–114.
KREBS, C.; WEINBERG, J.; AKESSON, E. Neurciências ilustrada. Porto Alegre: Artmed, 2013.
LEE, J.H.; LEE, S.; KIN, J. Amygdala Circuits for Fear Memory: A Key Role for Dopamine Regulation.The Neuroscientist, 2016, p.1-12.
LEMOS, N.A.M. Expressão de Zif-268 na aquisição, evocação e extinção de uma memória aversiva. Dissertação (Mestrado em Psicobiologia). Centro de Biociências. Universidade Federal do Rio Grande do Norte. 2008.
LENT, R. 100 bilhões de neurônios. Rio de Janeiro: Editora Atheneu, 2010.
LEVENSON, R.W. The autonomic nervous system and emotion. Emotion Review, 2014, vol.6, n.2, p.100 –112.
MAREN, S.; JIN, J. Prefrontal-hippocampal interactions in memory and emotion. Frontiers in Systems Neuroscience. 2015, vol.9, n.170, p.1-8.
McDermott, K.B.; Roediger, H.L. Memory (encoding, storage, retrieval). In: Biswas-Diener, R.; Diener, E. (Eds). Noba textbook series: Psychology. Champaign, IL: DEF publishers, 2017.
MCGAUGH, J.L. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci., 2004, vol.27, p.1–28.
MCGAUGH, J.L. Emotional arousal and enhanced amygdala activity: New evidence for the old perseveration-consolidation hypothesis. Learn. Mem., 2005, vol.12, p.77-79.
MCGAUGH, J.L. Making lasting memories: Remembering the significant. PNAS, 2013, vol. 110, n.2, p.10402–10407.
MCINTYRE, C.K.; ROOZENDAALL, B.; MCGAUGH, J.L. Role of the basolateral amigdala in memory consolidation. Ann N Y Acad Sci., 2003, vol.985, p.273-93.
Menezes, J.; Alves, N.; Borges, S.; Roehrs, R.; Myskiw, J.C.; FurinI, C.R.G. Facilitation of fear extinction by novelty depends on dopamine acting on D1-subtype dopamine receptors in hippocampus. Proc. Natl. Acad. Sci. USA., 2015, vol.112, p.E1652–E1658.
Milad, M.R., Pitman, R.K., Ellis, C.B., Gold, A.L., Shin, L.M., Lasko, N.B., Rauch, S.L. Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder. Biol Psychiatry., 2009, vol.66, n.12, p.1075–1082.
MILEYKOVSKIY, B.; MORALES, M. Duration of inhibition of ventral tegmental area dopamine neurons encodes a level of conditioned fear. J Neurosci., v.31, n.20, p.7471–7476, 2011.
Moustafa, A.A.; Gilbertson, M.W.; Orr, S.P.; Herzallah, M.M.; Servatius, R.J.; MyerS, C.E. A model of amygdala-hippocampal-prefrontal interaction in fear conditioning and extinction in animals. Brain Cogn., v.81, n.1, p.29–43, 2013.
MUELLER, D.; BRAVO-RIVERA, C.; QUIRK, G.J. Infralimbic D2 receptors are necessary for fear extinction and extinction-related tone responses. Biol Psychiatry. v.68, n.11, p.1055–1060, 2010.
NASSER, H. M. et al. The dopamine prediction error: contributions to associative models of reward learning. Frontiers in psychology, v. 8, p. 244, 2017.
NOBILI, A. et al. Dopamine neuronal loss contributes to memory and reward dysfunction in a model of Alzheimer's disease. Nature Communications, 2017, vol.8, n.14727, p.1-14.
NORMAN, G.J.; BERNTSON, G.G.; CACIOPPO, J.T. Emotion, somatovisceral afference, and autonomic regulation. Emotion Review, 2014, vol.6, n.2, p.113 –123.
Ortiz, O.; Delgado-Garcia, J.M.; Espadas, I.; Bahi, A.; Trullas, R.; Dreyer, J.L.; Moratalla, R. Associative learning and CA3-CA1 synaptic plasticity are impaired in D1R null, Drd1a−/− mice and in hippocampal siRNA silenced Drd1a mice. J Neurosci., 2010, vol.30, n.37, p.12288–12300.
Ouyang, M.; Young, M.B.; Lestini, M.M.; Schutsky, K.; Thomas, S.A. Redundant catecholamine signaling consolidates fear memory via phospholipase C. J Neurosci., 2012, vol.32, n.6, p.1932–1941.
PARÉ, D. Role of the basolateral amygdala in memory consolidation. Progress in Neurobiology, 2003, vol.70, p.409–420.
PATTON, M.H.; BIZUP, B.T.; GRACE, A.A. The infralimbic cortex bidirectionally modulates mesolimbic dopamine neuron activity via distinct neural pathways. J Neurosci., 2013, vol.33, n.43, p.16865–16873.
PERGHER, G.K. et al. Memória, humor e emoção. Rev Psiquiatr RS, 2006, vol.28, n.1, p.61-68.
PEZZE, M.A.; FELDON, J. Mesolimbic dopaminergic pathways in fear conditioning. Prog Neurobiol., 2004, vol.74, n.5, p.301–320.
Pezze, M.A.; BAST, T.; FELDON, J. Significance of dopamine transmission in the rat medial prefrontal cortex for conditioned fear. Cereb Cortex., 2003, vol.13, n.4, p.371–380.
Pezze, M.A.; Heidbreder, C.A.; Feldon, J.; Murphy, C.A. Selective responding of nucleus accumbens core and shell dopamine to aversively conditioned contextual and discrete stimuli. Neuroscience., 2001, vol.108, n.1, p.91–102.
PHELPS, E.A.; DELGADO, M.R.; NEARING, K.; LEDOUX, J.E. Extinction Learning in Humans: Role of the Amygdala and vmPFC. Neuron, 2004, vol. 43, p.897–905.
PHELPS, E.A.; LEDOUX, J.E. Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron, v.48, p.175–187, 2005.
PITMAN, et al. Biological studies of post-traumatic stress disorder. Nature Reviews Neuroscience, 2012, vol.13, p.769-787.
Ponnusamy, R.; Nissim, H.A.; Barad, M. Systemic blockade of D2-like dopamine receptors facilitates extinction of conditioned fear in mice. Learn Mem., 2005, vol.12, n.4, p.399–406.
QUIRK, G.J.; MUELLER, D. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology., 2008, vol.33, n.1, p.56–72.
RASHID, A.J. et al. Competition between engrams influences fear memory formation and recall. Science, 2016, vol.353, n.6297, p.383-387.
Reynolds, S.M.; Berridge, K.C. Emotional environments retune the valence of appetitive versus fearful functions in nucleus accumbens. Nat Neurosci., 2008, vol.11, n.4, p.423–425.
Richard, J.M.; Berridge, K.C. Nucleus accumbens dopamine/glutamate interaction switches modes to generate desire versus dread: D(1) alone for appetitive eating but D(1) and D(2) together for fear. J Neurosci., 2011, vol.31, n.36, p.12866–12879.
Rodriguez-Romaguera, J.; Do Monte, F.H.; Quirk, G.J. Deep brain stimulation of the ventral striatum enhances extinction of conditioned fear. Proc Natl Acad Sci USA., 2012, vol.109, n.22, p.8764–8769.
ROOZENDAALL, B.; MCGAUGH, J.L. Memory modulation. Behav Neurosci., 2011, vol.125, n.6, p.797–824. doi:10.1037/a0026187.
ROSENKRANZ, J.A.; GRACE, A.A. Cellular mechanisms of infralimbic and prelimbic prefrontal cortical inhibition and dopaminergic modulation of basolateral amygdala neurons in vivo. J Neurosci., 2002, vol.22, n.1, p.324–337.
Rossato, J.I.; Bevilaqua, L.R.; Izquierdo, I.; Medina, J.H.; CammarotA, M. Dopamine controls persistence of long-term memory storage. Science., 2009, vol.325, n.5943, p.1017–1020.
SALAMONE, J.D.; CORREA, M. The mysterious motivational functions of mesolimbic dopamine. Neuron, v. 76, n. 3, p. 470-485, 2012.
SCHULTZ, W. Behavioral dopamine signals. TRENDS in Neurosciences, 2007, vol.30, n.5, doi:10.1016/j.tins.2007.03.007.
SCHULTZ, W. Dopamine signals for reward value and risk: basic and recent data. Behav. Brain Funct, 2010, vol.6, n.24.
SCHULTZ, W. NEURONAL REWARD AND DECISION SIGNALS: FROM THEORIES TO DATA. Physiol Rev, 2015, vol.95, p.853–951.
SCHULTZ, W. Dopamine reward predictionerror signalling: a two-component response. Nature Reviews Neuroscience, 2016, vol. 17, p. 183-195.
SHIN, L.M.; RAUCH, S.L.; PITMAN, R.K. Amygdala, medial prefrontal cortex, and hippocampal function in PTSD. Ann N Y Acad Sci., 2006, vol.1071, p.67–79.
TOVOTE, P.; FADOK, J.P.; LUTHI, A. Neuronal circuits for fear and anxiety. Nature, 2015, vol.16, p.317-331.
Valenti, O.; Lodge, D.J.; Grace, A.A. Aversive stimuli alter ventral tegmental area dopamine neuron activity via a common action in the ventral hippocampus. J Neurosci., 2011, vol.31, n.11, p.4280–4289.
VALJENT, E.; PASCOLI, V.; SVENNINGSSON, P.; PAUL, S.; ENSLEN, H.; CORVOL, J.C.; GIRALT, J.A. Regulation of a protein phosphatase cascade allows convergent dopamine and glutamate signals to activate ERK in the striatum. Proc Natl Acad Sci USA., 2005, vol.102, n.2, p.491–496.
VERGARA, M.D. et al. Activation of type 4 dopaminergic receptors in the prelimbic area of medial prefrontal cortex is necessary for the expression of innate fear behavior. Behavioural brain research, 2017, vol. 324, p.130-137.
Weiner, D.M.; Levey, A.I.; Sunahara, R.K.; Niznik, H.B.; O'Dowd, B.F.; Seeman, P.; BranN, M.R. D1 and D2 dopamine receptor mRNA in rat brain. Proc Natl Acad Sci USA., 1991, vol.88, n.5, p.1859–1863.
XU, T.X.; YAO, W.D. D1 and D2 dopamine receptors in separate circuits cooperate to drive associative long-term potentiation in the prefrontal cortex. Proc Natl Acad Sci USA., 2010, vol.107, n.37, p.16366– 16371.
YERKES, R.M.; DODSON, J.D. The relation of strength of stimulus to rapidity of habit-formation. Journal of Comparative Neurology and Psychology, 1908, vol.18, n.459e482, p.459−482, doi:10.1002/ cne.920180503.
YIN, H.H.; OSTLUND, S.B.; BALLEINE, B.W. Reward-guided learning beyond dopamine in the nucleus accumbens: the integrative functions of cortico-basal ganglia networks. Eur. J. Neurosci., 2008, vol.28, p.1437–1448.
Downloads
Publicado
Como Citar
Edição
Seção
Licença
A revista se reserva o direito de fazer alterações nas regras originais, na ortografia e na ordem gramatical, a fim de manter o idioma de culto padrão, respeitando, no entanto, o estilo dos autores. Os artigos publicados são de propriedade da revista Scientific Electronic Archives, tornando-se sua reimpressão total ou parcial, sujeitos à autorização expressa da direção da revista. A fonte original da publicação deve ser mantida. Os originais não serão devolvidos aos autores. As opiniões expressas pelos autores dos artigos são de sua exclusiva responsabilidade.
The journal reserves the right to make changes to the original rules, spelling and grammatical order, in order to keep the language of worship default, respecting, however, the style of the authors. Articles published are the property of Scientific Electronic Archives magazine, becoming its total or partial reprint, subject to the express authorization of the direction of the journal. The original source of publication should be retained. The originals will not be returned to the authors. Opinions expressed by authors of articles are solely your responsibility.
This journal uses the License Creative Commons Atribuição 4.0 Internacional.
