Computational search for hypotheses concerning the endocannabinoid contribution to the extinction of fear conditioning

Frontiers in Computational Neuroscience

Volumn , Issue MAY, 2013, Pages

  Anastasio, Thomas J ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Declarative programming; Endocannabinoids; Extinction of fear conditioning; Formal methods; Neural networks; State space search

Indexed keywords

COMPUTATIONAL ANALYSIS; DECLARATIVE PROGRAMMING; ENDOCANNABINOIDS; GABAERGIC SYNAPSIS; INHIBITORY INTERNEURONS; LONG TERM DEPRESSION; STATE-SPACE; SYNAPTIC STRENGTHS;

FORMAL METHODS; LOGIC PROGRAMMING; NEURAL NETWORKS;

NEURONS;

CANNABINOID 1 RECEPTOR; ENDOCANNABINOID;

ARTICLE; ASSOCIATION; BASOLATERAL AMYGDALA; CONDITIONING; FEAR; FEAR CONDITIONING; GABAERGIC SYSTEM; INTERNEURON; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MEMORY CONSOLIDATION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE PROJECTION; REINFORCEMENT; SYNAPSE;

EID: 84877986540     PISSN: 16625188     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncom.2013.00074     Document Type: Article

References (81)

1. Amano, T., Unal, C.T., and Pare, D. (2010). Synaptic correlates of fear extinction in the amygdala. Nat Neurosci 13, 489-494.
2. Anastasio, T.J. (2010). Tutorial on Neural Systems Modeling. Sunderland, MA: Sinauer.
3. Anastasio, T.J. (2011). Data-driven modeling of Alzheimer disease pathogenesis. J Theor Biol 290, 60-72.
4. Anastasio, T.J. (2013). Exploring the contribution of estrogen to amyloid-Beta regulation: a novel multifactorial computational modeling approach. Front Pharmacol 4, 16.
5. Anglada-Figueroa, D., and Quirk, G.J. (2005). Lesions of the basal amygdala block expression of conditioned fear but not extinction. J Neurosci 25, 9680-9685.
6. Arenos, J.D., Musty, R.E., and Bucci, D.J. (2006). Blockade of cannabinoid CB1 receptors alters contextual learning and memory. Eur J Pharmacol 539, 177-183.
7. Azad, S.C., Eder, M., Marsicano, G., Lutz, B., Zieglgansberger, W., and Rammes, G. (2003). Activation of the cannabinoid receptor type 1 decreases glutamatergic and GABAergic synaptic transmission in the lateral amygdala of the mouse. Learn Mem 10, 116-128.
8. Azad, S.C., Monory, K., Marsicano, G., Cravatt, B.F., Lutz, B., Zieglgansberger, W., and Rammes, G. (2004). Circuitry for associative plasticity in the amygdala involves endocannabinoid signaling. J Neurosci 24, 9953-9961.
9. Bauer, E.P., and Ledoux, J.E. (2004). Heterosynaptic long-term potentiation of inhibitory interneurons in the lateral amygdala. J Neurosci 24, 9507-9512.
10. Bauer, E.P., Schafe, G.E., and Ledoux, J.E. (2002). NMDA receptors and L-type voltage-gated calcium channels contribute to long-term potentiation and different components of fear memory formation in the lateral amygdala. J Neurosci 22, 5239-5249.
11. Bitencourt, R.M., Pamplona, F.A., and Takahashi, R.N. (2008). Facilitation of contextual fear memory extinction and anti-anxiogenic effects of AM404 and cannabidiol in conditioned rats. Eur Neuropsychopharmacol 18, 849-859.
12. Blair, H.T., Schafe, G.E., Bauer, E.P., Rodrigues, S.M., and Ledoux, J.E. (2001). Synaptic plasticity in the lateral amygdala: a cellular hypothesis of fear conditioning. Learn Mem 8, 229-242.
13. Calandreau, L., Desmedt, A., Decorte, L., and Jaffard, R. (2005). A different recruitment of the lateral and basolateral amygdala promotes contextual or elemental conditioned association in Pavlovian fear conditioning. Learn Mem 12, 383-388.
14. Chapman, P.F., Kairiss, E.W., Keenan, C.L., and Brown, T.H. (1990). Long-term synaptic potentiation in the amygdala. Synapse 6, 271-278.
15. Chen, Z., Putrino, D.F., Ghosh, S., Barbieri, R., and Brown, E.N. (2011). Statistical inference for assessing functional connectivity of neuronal ensembles with sparse spiking data. IEEE Trans Neural Syst Rehabil Eng 19, 121-135.
16. Chhatwal, J.P., Davis, M., Maguschak, K.A., and Ressler, K.J. (2005). Enhancing cannabinoid neurotransmission augments the extinction of conditioned fear. Neuropsychopharmacology 30, 516-524.
17. Ciocchi, S., Herry, C., Grenier, F., Wolff, S.B., Letzkus, J.J., Vlachos, I., Ehrlich, I., Sprengel, R., Deisseroth, K., Stadler, M.B., Muller, C., and Luthi, A. (2010). Encoding of conditioned fear in central amygdala inhibitory circuits. Nature 468, 277-282.
18. Clavel, M., Durán, R., Eker, S., Lincoln, P., Martí-Oliet, N., Meseguer, J., and Talcott, C. (2007). All About Maude - A High-Preformance Logical Framework: How to Specify, Program, and Verify Systems in Rewriting Logic. Berlin: Springer.
19. Da Costa Gomez, T.M., and Behbehani, M.M. (1995). An electrophysiological characterization of the projection from the central nucleus of the amygdala to the periaqueductal gray of the rat: the role of opioid receptors. Brain Res 689, 21-31.
20. Eker, S., Knapp, M., Laderoute, K., Lincoln, P., and Talcott, C. (2004). Pathway logic: executable models of biological networks. Electronic Notes in Theoretical Computer Science 71, 144-161.
21. Fisher, J., and Henzinger, T.A. (2007). Executable cell biology. Nat Biotechnol 25, 1239-1249.
22. Ganon-Elazar, E., and Akirav, I. (2009). Cannabinoid receptor activation in the basolateral amygdala blocks the effects of stress on the conditioning and extinction of inhibitory avoidance. J Neurosci 29, 11078-11088.
23. Hempel, C.M., Sugino, K., and Nelson, S.B. (2002). Multi-unit spike-triggered averaging: a method for probing the physiology of central synapses. J Neurosci Methods 120, 121-129.
24. Herry, C., Ciocchi, S., Senn, V., Demmou, L., Muller, C., and Luthi, A. (2008). Switching on and off fear by distinct neuronal circuits. Nature 454, 600-606.
25. Herry, C., Ferraguti, F., Singewald, N., Letzkus, J.J., Ehrlich, I., and Luthi, A. (2010). Neuronal circuits of fear extinction. Eur J Neurosci 31, 599-612.
26. Hlavacek, W.S., Faeder, J.R., Blinov, M.L., Posner, R.G., Hucka, M., and Fontana, W. (2006). Rules for modeling signal-transduction systems. Sci STKE 2006, re6.
27. Hobin, J.A., Goosens, K.A., and Maren, S. (2003). Context-dependent neuronal activity in the lateral amygdala represents fear memories after extinction. J Neurosci 23, 8410-8416.
28. Holter, S.M., Kallnik, M., Wurst, W., Marsicano, G., Lutz, B., and Wotjak, C.T. (2005). Cannabinoid CB1 receptor is dispensable for memory extinction in an appetitively-motivated learning task. Eur J Pharmacol 510, 69-74.
29. Huang, Y.Y., and Kandel, E.R. (1998). Postsynaptic induction and PKA-dependent expression of LTP in the lateral amygdala. Neuron 21, 169-178.
30. Hurley, K.M., Herbert, H., Moga, M.M., and Saper, C.B. (1991). Efferent projections ofthe infralimbic cortex of the rat. J Comp Neurol 308, 249-276.
31. Huth, M., and Ryan, M. (2004). Logic in Computer Science: Modelling and Reasoning about Systems. Cambridge: Cambridge University Press.
32. Kamprath, K., Marsicano, G., Tang, J., Monory, K., Bisogno, T., Di Marzo, V., Lutz, B., and Wotjak, C.T. (2006). Cannabinoid CB1 receptor mediates fear extinction via habituation-like processes. J Neurosci 26, 6677-6686.
33. Katona, I., Rancz, E.A., Acsady, L., Ledent, C., Mackie, K., Hajos, N., and Freund, T.F. (2001). Distribution of CB1 cannabinoid receptors in the amygdala and their role in the control of GABAergic transmission. J Neurosci 21, 9506-9518.
34. Krasne, F.B., Fanselow, M.S., and Zelikowsky, M. (2011). Design of a neurally plausible model of fear learning. Front Behav Neurosci 5, 41.
35. Krettek, J.E., and Price, J.L. (1978). A description of the amygdaloid complex in the rat and cat with observations on intra-amygdaloid axonal connections. J Comp Neurol 178, 255-280.
36. Lafenetre, P., Chaouloff, F., and Marsicano, G. (2007). The endocannabinoid system in the processing of anxiety and fear and how CB1 receptors may modulate fear extinction. Pharmacol Res 56, 367-381.
37. Ledoux, J.E. (2000). Emotion circuits in the brain. Annu Rev Neurosci 23, 155-184.
38. Ledoux, J.E., Cicchetti, P., Xagoraris, A., and Romanski, L.M. (1990). The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning. J Neurosci 10, 1062-1069.
39. Likhtik, E., Pelletier, J.G., Paz, R., and Pare, D. (2005). Prefrontal control of the amygdala. J Neurosci 25, 7429-7437.
40. Likhtik, E., Popa, D., Apergis-Schoute, J., Fidacaro, G.A., and Pare, D. (2008). Amygdala intercalated neurons are required for expression of fear extinction. Nature 454, 642-645.
41. Linke, R., Braune, G., and Schwegler, H. (2000). Differential projection of the posterior paralaminar thalamic nuclei to the amygdaloid complex in the rat. Exp Brain Res 134, 520-532.
42. Mahan, A.L., and Ressler, K.J. (2012). Fear conditioning, synaptic plasticity and the amygdala: implications for posttraumatic stress disorder. Trends Neurosci 35, 24-35.
43. Mahanty, N.K., and Sah, P. (1998). Calcium-permeable AMPA receptors mediate long-term potentiation in interneurons in the amygdala. Nature 394, 683-687.
44. Maren, S. (1999). Long-term potentiation in the amygdala: a mechanism for emotional learning and memory. Trends Neurosci 22, 561-567.
45. Marsicano, G., Wotjak, C.T., Azad, S.C., Bisogno, T., Rammes, G., Cascio, M.G., Hermann, H., Tang, J., Hofmann, C., Zieglgansberger, W., Di Marzo, V., and Lutz, B. (2002). The endogenous cannabinoid system controls extinction of aversive memories. Nature 418, 530-534.
46. Mcdonald, A.J. (1985). Immunohistochemical identification of gamma-aminobutyric acid-containing neurons in the rat basolateral amygdala. Neurosci Lett 53, 203-207.
47. Mcdonald, A.J. (1998). Cortical pathways to the mammalian amygdala. Prog Neurobiol 55, 257-332.
48. Mcdonald, A.J., and Mascagni, F. (2001). Localization of the CB1 type cannabinoid receptor in the rat basolateral amygdala: high concentrations in a subpopulation of cholecystokinin-containing interneurons. Neuroscience 107, 641-652.
49. Mcdonald, A.J., Mascagni, F., and Guo, L. (1996). Projections of the medial and lateral prefrontal cortices to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience 71, 55-75.
50. Mckernan, M.G., and Shinnick-Gallagher, P. (1997). Fear conditioning induces a lasting potentiation of synaptic currents in vitro. Nature 390, 607-611.
51. Milad, M.R., and Quirk, G.J. (2002). Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 420, 70-74.
52. Milad, M.R., Vidal-Gonzalez, I., and Quirk, G.J. (2004). Electrical stimulation of medial prefrontal cortex reduces conditioned fear in a temporally specific manner. Behav Neurosci 118, 389-394.
53. Myers, K.M., and Davis, M. (2007). Mechanisms of fear extinction. Mol Psychiatry 12, 120-150.
54. Nader, K., Majidishad, P., Amorapanth, P., and Ledoux, J.E. (2001). Damage to the lateral and central, but not other, amygdaloid nuclei prevents the acquisition of auditory fear conditioning. Learn Mem 8, 156-163.
55. Niyuhire, F., Varvel, S.A., Thorpe, A.J., Stokes, R.J., Wiley, J.L., and Lichtman, A.H. (2007). The disruptive effects of the CB1 receptor antagonist rimonabant on extinction learning in mice are task-specific. Psychopharmacology (Berl) 191, 223-231.
56. Onishi, B.K., and Xavier, G.F. (2010). Contextual, but not auditory, fear conditioning isdisrupted by neurotoxic selective lesion of the basal nucleus of amygdala in rats. Neurobiol Learn Mem 93, 165-174.
57. Pare, D., and Duvarci, S. (2012). Amygdala microcircuits mediating fear expression and extinction. Curr Opin Neurobiol.
58. Pare, D., Quirk, G.J., and Ledoux, J.E. (2004). New vistas on amygdala networks in conditioned fear. J Neurophysiol 92, 1-9.
59. Pare, D., and Smith, Y. (1993). The intercalated cell masses project to the central and medial nuclei of the amygdala in cats. Neuroscience 57, 1077-1090.
60. Pare, D., Smith, Y., and Pare, J.F. (1995). Intra-amygdaloid projections of the basolateral and basomedial nuclei in the cat: Phaseolus vulgaris-leucoagglutinin anterograde tracing at the light and electron microscopic level. Neuroscience 69, 567-583.
61. Piomelli, D. (2003). The molecular logic of endocannabinoid signalling. Nat Rev Neurosci 4, 873-884.
62. Pitkanen, A., and Amaral, D.G. (1991). Demonstration of projections from the lateral nucleus to the basal nucleus of the amygdala: a PHA-L study in the monkey. Exp Brain Res 83, 465-470.
63. Pitkanen, A., Savander, V., and Ledoux, J.E. (1997). Organization of intra-amygdaloid circuitries in the rat: an emerging framework for understanding functions of theamygdala. Trends Neurosci 20, 517-523.
64. Quirk, G.J., Likhtik, E., Pelletier, J.G., and Pare, D. (2003). Stimulation of medial prefrontal cortex decreases the responsiveness of central amygdala output neurons. J Neurosci 23, 8800-8807.
65. Rammes, G., Steckler, T., Kresse, A., Schutz, G., Zieglgansberger, W., and Lutz, B. (2000). Synaptic plasticity in the basolateral amygdala in transgenic mice expressing dominant-negative cAMP response element-binding protein (CREB) in forebrain. Eur J Neurosci 12, 2534-2546.
66. Repa, J.C., Muller, J., Apergis, J., Desrochers, T.M., Zhou, Y., and Ledoux, J.E. (2001). Two different lateral amygdala cell populations contribute to the initiation and storage of memory. Nat Neurosci 4, 724-731.
67. Rizvi, T.A., Ennis, M., Behbehani, M.M., and Shipley, M.T. (1991). Connections between the central nucleus of the amygdala and the midbrain periaqueductal gray: topography and reciprocity. J Comp Neurol 303, 121-131.
68. Rogan, M.T., and Ledoux, J.E. (1995). LTP is accompanied by commensurate enhancement of auditory-evoked responses in a fear conditioning circuit. Neuron 15, 127-136.
69. Rosenkranz, J.A., and Grace, A.A. (2001). Dopamine attenuates prefrontal cortical suppression of sensory inputs to the basolateral amygdala of rats. J Neurosci 21, 4090-4103.
70. Rosenkranz, J.A., and Grace, A.A. (2002). Cellular mechanisms of infralimbic and prelimbic prefrontal cortical inhibition and dopaminergic modulation of basolateral amygdala neurons in vivo. J Neurosci 22, 324-337.
71. Rosenkranz, J.A., Moore, H., and Grace, A.A. (2003). The prefrontal cortex regulateslateral amygdala neuronal plasticity and responses to previously conditioned stimuli. J Neurosci 23, 11054-11064.
72. Royer, S., Martina, M., and Pare, D. (1999). An inhibitory interface gates impulse traffic between the input and output stations of the amygdala. J Neurosci 19, 10575-10583.
73. Royer, S., Martina, M., and Pare, D. (2000). Polarized synaptic interactions between intercalated neurons of the amygdala. J Neurophysiol 83, 3509-3518.
74. Royer, S., and Pare, D. (2002). Bidirectional synaptic plasticity in intercalated amygdale neurons and the extinction of conditioned fear responses. Neuroscience 115, 455-462.
75. Shumyatsky, G.P., Tsvetkov, E., Malleret, G., Vronskaya, S., Hatton, M., Hampton, L., Battey, J.F., Dulac, C., Kandel, E.R., and Bolshakov, V.Y. (2002). Identification of a signaling network in lateral nucleus of amygdala important for inhibiting memory specifically related to learned fear. Cell 111, 905-918.
76. Sotres-Bayon, F., Bush, D.E., and Ledoux, J.E. (2004). Emotional perseveration: an update on prefrontal-amygdala interactions in fear extinction. Learn Mem 11, 525-535.
77. Talcott, C. (2008). Pathway logic, in: Lecture Notes in Computer Science 5016. (eds.) M. Bernardo, P. Degano & G. Zavattaro.).
78. Turner, B.H., and Herkenham, M. (1991). Thalamoamygdaloid projections in the rat: a test of the amygdala's role in sensory processing. J Comp Neurol 313, 295-325.
79. Vlachos, I., Herry, C., Luthi, A., Aertsen, A., and Kumar, A. (2011). Context-dependent encoding of fear and extinction memories in a large-scale network model of the basal amygdala. PLoS Comput Biol 7, e1001104.
80. Woodson, W., Farb, C.R., and Ledoux, J.E. (2000). Afferents from the auditory thalamus synapse on inhibitory interneurons in the lateral nucleus of the amygdala. Synapse 38, 124-137.
81. Zimmerman, J.M., and Maren, S. (2010). NMDA receptor antagonism in the basolateral but not central amygdala blocks the extinction of Pavlovian fear conditioning in rats. Eur J Neurosci 31, 1664-1670.