Altering D1 receptor activity in the basolateral amygdala impairs fear suppression during a safety cue

Neurobiology of Learning and Memory

Volumn 147, Issue , 2018, Pages 26-34

  Ng, Ka H ^a,b   Pollock, Michael W ^a   Urbanczyk, Phillip J ^a   Sangha, Susan ^a,b  

^a PURDUE UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

Author keywords

Amygdala; Dopamine; Fear; Safety

Indexed keywords

DOPAMINE 1 RECEPTOR; 2,3,4,5 TETRAHYDRO 7,8 DIHYDROXY 1 PHENYL 1H 3 BENZAZEPINE; 8 CHLORO 2,3,4,5 TETRAHYDRO 3 METHYL 5 PHENYL 1H 3 BENZAZEPIN 7 OL HYDROGEN MALEATE; BENZAZEPINE DERIVATIVE; DOPAMINE RECEPTOR BLOCKING AGENT; DOPAMINE RECEPTOR STIMULATING AGENT;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASSOCIATION; BASOLATERAL AMYGDALA; CONTROLLED STUDY; FEAR; LOCOMOTION; MALE; MOTIVATION; NEUROMODULATION; NONHUMAN; PERCEPTIVE DISCRIMINATION; RAT; REINFORCEMENT; REWARD; SAFETY; ANIMAL; DISCRIMINATION LEARNING; DRUG EFFECT; LONG EVANS RAT;

2,3,4,5-TETRAHYDRO-7,8-DIHYDROXY-1-PHENYL-1H-3-BENZAZEPINE; ANIMALS; BASOLATERAL NUCLEAR COMPLEX; BEHAVIOR, ANIMAL; BENZAZEPINES; CUES; DISCRIMINATION LEARNING; DOPAMINE AGONISTS; DOPAMINE ANTAGONISTS; FEAR; MALE; RATS; RATS, LONG-EVANS; RECEPTORS, DOPAMINE D1; REWARD; SAFETY;

EID: 85035055119     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2017.11.011     Document Type: Article

References (32)

1. Abraham, A., Neve, K., Lattal, K., Dopamine and extinction: A convergence of theory with fear and reward circuitry. Neurobiology of Learning and Memory, 2014.
2. Blanchard, R.J., Blanchard, D.C., Crouching as an index of fear. Journal of Comparative and Physiological Psychology 67:3 (1969), 370–375.
3. Collins, A. L., Greenfield, V. Y., Bye, J. K., Linker, K. E., Wang, A. S., & Wassum, K. M. (2016). Dynamic mesolimbic dopamine signaling during action sequence learning and expectation violation. Scientific Reports, 6(October 2015), 20231. https://doi.org/10.1038/srep20231.
4. de Oliveira, A.R., Reimer, A.E., De Macedo, C.E.A., De Carvalho, M.C., Silva, M.A.D.S., Brandão, M.L., Conditioned fear is modulated by D2 receptor pathway connecting the ventral tegmental area and basolateral amygdala. Neurobiology of Learning and Memory 95:1 (2011), 37–45, 10.1016/j.nlm.2010.10.005.
5. Doty, R.L., Li, C., Bagla, R., Huang, W., Pfeiffer, C., Brosvic, G.M., Risser, J.M., SKF 38393 enhances odor detection performance. Psychopharmacology (Berl) 136:1 (1998), 75–82.
6. Eagle, A.L., Olumolade, O.O., Otani, H., Partial dopaminergic denervation-induced impairment in stimulus discrimination acquisition in parkinsonian rats: A model for early Parkinson's disease. Neuroscience Research 92 (2014), 1–9, 10.1016/j.neures.2014.11.002.
7. Fendt, M., Fanselow, M.S., The neuroanatomical and neurochemical basis of conditioned fear. Neuroscience & Biobehavioral Reviews 23:5 (1999), 743–760, 10.1016/S0149-7634(99)00016-0.
8. Forbes, M.K., Flanagan, J.C., Barrett, E.L., Crome, E., Baillie, A.J., Mills, K.L., Teesson, M., Smoking, posttraumatic stress disorder, and alcohol use disorders in a nationally representative sample of Australian men and women. Drug and Alcohol Dependence 156 (2015), 176–183, 10.1016/j.drugalcdep.2015.09.007.
9. 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. Neurobiology of Learning and Memory 90:1 (2008), 217–222, 10.1016/j.nlm.2008.03.003.
10. Holtzman-Assif, O., Laurent, V., Westbrook, R.F., Blockade of dopamine activity in the nucleus accumbens impairs learning extinction of conditioned fear. Learning and Memory 17:2 (2010), 71–75.
11. Inoue, T., Izumi, T., Maki, Y., Muraki, I., Koyama, T., Effect of the dopamine D(1/5) antagonist SCH 23390 on the acquisition of conditioned fear. Pharmacology, Biochemistry, and Behavior 66:3 (2000), 573–578.
12. Jones, J.L., Day, J.J., Aragona, B.J., Wheeler, R.A., Wightman, R.M., Carelli, R.M., Basolateral amygdala modulates terminal dopamine release in the nucleus accumbens and conditioned responding. Biological Psychiatry 67:8 (2010), 737–744, 10.1016/j.biopsych.2009.11.006.
13. Jovanovic, T., Norrholm, S.D., Fennell, J.E., Keyes, M., Fiallos, A.M., Myers, K.M., Duncan, E.J., Posttraumatic stress disorder may be associated with impaired fear inhibition: Relation to symptom severity. Psychiatry Research 167:1–2 (2009), 151–160, 10.1016/j.psychres.2007.12.014.
14. Kessler, R.C., Berglund, P., Demler, O., Jin, R., Merikangas, K.R., Walters, E.E., Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the national comorbidity survey replication. Archives of General Psychiatry 62:June (2005), 593–602, 10.1001/archpsyc.62.6.593.
15. Larkin, J.D., Jenni, N.L., Floresco, S.B., Modulation of risk/reward decision making by dopaminergic transmission within the basolateral amygdala. Psychopharmacology (Berl) 233:1 (2016), 121–136, 10.1007/s00213-015-4094-8.
16. Li, C., Rainnie, D.G., Bidirectional regulation of synaptic plasticity in the basolateral amygdala induced by the D1-like family of dopamine receptors and group II metabotropic glutamate receptors. Journal of Physiology 592:19 (2014), 4329–4351.
17. Morriss, J., Christakou, A., Van Reekum, C.M., Intolerance of uncertainty predicts fear extinction in amygdala-ventromedial prefrontal cortical circuitry. Biology of Mood & Anxiety Disorders, 5(1), 2015, 4, 10.1186/s13587-015-0019-8.
18. Ouimette, P., Read, JP., Wade, M., Tirone, V., Modeling associations between posttraumatic stress symptoms and substance use. Addictive Behaviors, 35, 2010.
19. Pezze, M.A., Marshall, H.J., Cassaday, H.J., The dopamine D1 receptor agonist SKF81297 has dose-related effects on locomotor activity but is without effect in a CER trace conditioning procedure conducted with two versus four trials. Learning and Motivation 55 (2016), 53–64, 10.1016/j.lmot.2016.06.001.
20. Richard, J.M., Berridge, K.C., Nucleus accumbens dopamine/glutamate interaction switches modes to generate desire versus dread: D1 alone for appetitive eating but D1 and D2 together for fear. Journal of Neuroscience 31:36 (2011), 12866–12879, 10.1523/JNEUROSCI.1339-11.2011.
21. Rogan, M.T., Leon, K.S., Perez, D.L., Kandel, E.R., Distinct neural signatures for safety and danger in the amygdala and striatum of the mouse. Neuron 46:2 (2005), 309–320, 10.1016/j.neuron.2005.02.017.
22. Sangha, S., Plasticity of fear and safety neurons of the amygdala in response to fear extinction. Frontiers in Behavioral Neuroscience 9:December (2015), 1–10, 10.3389/fnbeh.2015.00354.
23. Sangha, S., Chadick, J.Z., Janak, P.H., Safety encoding in the basal amygdala. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 33:9 (2013), 3744–3751, 10.1523/JNEUROSCI.3302-12.2013.
24. Sangha, S., Greba, Q., Robinson, P.D., Ballendine, S.A., Howland, J.G., Heightened fear in response to a safety cue and extinguished fear cue in a rat model of maternal immune activation. Frontiers in Behavioral Neuroscience, 8(May), 2014, 168, 10.3389/fnbeh.2014.00168.
25. Sangha, S., Robinson, P.D., Greba, Q., Davies, D.A., Howland, J.G., Alterations in reward, fear and safety cue discrimination after inactivation of the rat prelimbic and infralimbic cortices. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology 39:10 (2014), 2405–2413, 10.1038/npp.2014.89.
26. Sciascia, J.M., Mendoza, J., Chaudhri, N., Blocking dopamine d1-like receptors attenuates context-induced renewal of pavlovian-conditioned alcohol-seeking in rats. Alcoholism, Clinical and Experimental Research 38:2 (2014), 418–427, 10.1111/acer.12262.
27. Stuber, G.D., Sparta, D.R., Stamatakis, A.M., van Leeuwen, W.A., Hardjoprajitno, J.E., Cho, S., Bonci, A., Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking. Nature 475:7356 (2011), 377–380, 10.1038/nature10194.
28. Tobin, S., Sedki, F., Abbas, Z., Shalev, U., Antagonism of the dopamine D1-like receptor in mesocorticolimbic nuclei attenuates acute food deprivation-induced reinstatement of heroin seeking in rats. European Journal of Neuroscience 37:6 (2013), 972–981, 10.1111/ejn.12112.
29. Tran, A.H., Tamura, R., Uwano, T., Kobayashi, T., Katsuki, M., Ono, T., Dopamine D1 receptors involved in locomotor activity and accumbens neural responses to prediction of reward associated with place. Proceedings of the National Academy of Sciences of the United States of America 102:6 (2005), 2117–2122, 10.1073/pnas.0409726102.
30. Wassum, K.M., Izquierdo, A., The basolateral amygdala in reward learning and addiction. Neuroscience and Biobehavioral Reviews 57 (2015), 271–283, 10.1016/j.neubiorev.2015.08.017.
31. Weiner, D.M., Levey, A.I., Sunahara, R.K., Niznik, H.B., O'dowd, BF., Seeman, P., Brann, MR., D1 and D2 dopamine receptor mRNA in rat brain. Neurobiology 88 (1991), 1859–1863.
32. Zarrindast, M.-R., Rezayof, A., Sahraei, H., Haeri-Rohani, A., Rassouli, Y., Involvement of dopamine D1 receptors of the central amygdala on the acquisition and expression of morphine-induced place preference in rat. Brain Research 965:1 (2003), 212–221, 10.1016/S0006-8993(02)04201-4.