Connections of the Mouse Orbitofrontal Cortex and Regulation of Goal-Directed Action Selection by Brain-Derived Neurotrophic Factor

Biological Psychiatry

Volumn 81, Issue 4, 2017, Pages 366-377

  Zimmermann, Kelsey S ^a,b   Yamin, John A ^a,b   Rainnie, Donald G ^a,b   Ressler, Kerry J ^a,b,c   Gourley, Shannon L ^a,b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Action; Amygdala; Habit; Orbital; Outcome; Striatum

Indexed keywords

7,8 DIHYDROXYFLAVONE; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; FASUDIL; RHO KINASE; RHO KINASE INHIBITOR; VIRUS VECTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASOLATERAL AMYGDALA; BLOOD BRAIN BARRIER; BRAIN HISTOLOGY; CELL DENSITY; CELL PROLIFERATION; CONDITIONING; CONTROLLED STUDY; CORPUS STRIATUM; DECISION MAKING; DENDRITIC SPINE; DORSAL STRIATUM; ENZYME INHIBITION; FUNCTIONAL CONNECTIVITY; GENE SILENCING; HABIT; INSTRUMENTAL CONDITIONING; MALE; MOTIVATION; MOUSE; NERVE CELL PLASTICITY; NEURITE OUTGROWTH; NONHUMAN; ORBITAL CORTEX; PERIRHINAL CORTEX; PRELIMBIC CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; REINFORCEMENT; STIMULUS RESPONSE; VENTROLATERAL PREFRONTAL CORTEX; AMYGDALA; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CYTOLOGY; NERVE TRACT; NEUROANATOMICAL TRACT TRACING; PHYSIOLOGY; PREFRONTAL CORTEX;

AMYGDALA; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CONDITIONING, OPERANT; CORPUS STRIATUM; DECISION MAKING; EXTINCTION, PSYCHOLOGICAL; GOALS; HABITS; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NEURAL PATHWAYS; NEUROANATOMICAL TRACT-TRACING TECHNIQUES; PREFRONTAL CORTEX; RECEPTOR, TRKB;

EID: 84954357817     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2015.10.026     Document Type: Article

References (60)

1. 1 Rhodes, S.E., Murray, E.A., Differential effects of amygdala, orbital prefrontal cortex, and prelimbic cortex lesions on goal-directed behavior in rhesus macaques. J Neurosci 33 (2013), 3380–3389.
2. 2 McDannald, M.A., Jones, J.L., Takahashi, Y.K., Schoenbaum, G., Learning theory: A driving force in understanding orbitofrontal function. Neurobiol Learn Mem 108 (2014), 22–27.
3. 3 Padoa-Schioppa, C., Neurobiology of economic choice: A good-based model. Annu Rev Neurosci 34 (2011), 333–359.
4. 4 Schoenbaum, G., Roesch, M.R., Stalnaker, T.A., Takahashi, Y.K., A new perspective on the role of the orbitofrontal cortex in adaptive behaviour. Nat Rev Neurosci 10 (2009), 885–892.
5. 5 Gremel, C.M., Costa, R.M., Orbitofrontal and striatal circuits dynamically encode the shift between goal-directed and habitual actions. Nat Commun, 4, 2013, 2264.
6. 6 Ahmari, S.E., Spellman, T., Douglass, N.L., Kheirbek, M.A., Simpson, H.B., Deisseroth, K., et al. Repeated cortico-striatal stimulation generates persistent OCD-like behavior. Science 340 (2013), 1234–1239.
7. 7 Gourley, S.L., Olevska, A., Zimmermann, K.S., Ressler, K.J., Dileone, R.J., Taylor, J.R., The orbitofrontal cortex regulates outcome-based decision-making via the lateral striatum. Eur J Neurosci 38 (2013), 2382–2388.
8. 8 McDonald, A.J., Mascagni, F., Guo, L., Projections of the medial and lateral prefrontal cortices to the amygdala: A Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience 71 (1996), 55–75.
9. 9 Balleine, B.W., Killcross, A.S., Dickinson, A., The effect of lesions of the basolateral amygdala on instrumental conditioning. J Neurosci 23 (2003), 666–675.
10. 10 Wang, S.H., Ostlund, S.B., Nader, K., Balleine, B.W., Consolidation and reconsolidation of incentive learning in the amygdala. J Neurosci 25 (2005), 830–835.
11. 11 Shiflett, M.W., Balleine, B.W., At the limbic-motor interface: Disconnection of basolateral amygdala from nucleus accumbens core and shell reveals dissociable components of incentive motivation. Eur J Neurosci 32 (2010), 1735–1743.
12. 12 Corbit, L.H., Leung, B.K., Balleine, B.W., The role of the amygdala-striatal pathway in the acquisition and performance of goal-directed instrumental actions. J Neurosci 33 (2013), 17682–17690.
13. 13 Mailly, P., Aliane, V., Groenewegen, H.J., Haber, S.N., Deniau, J.M., The rat prefrontostriatal system analyzed in 3D: Evidence for multiple interacting functional units. J Neurosci 33 (2013), 5718–5727.
14. 14 Rios, M., Fan, G., Fekete, C., Kelly, J., Bates, B., Kuehn, R., et al. Conditional deletion of brain-derived neurotrophic factor in the postnatal brain leads to obesity and hyperactivity. Mol Endocrinol 15 (2001), 1748–1757.
15. 15 Feng, G., Mellor, R.H., Bernstein, M., Keller-Peck, C., Nguyen, Q.T., Wallace, M., et al. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28 (2000), 41–51.
16. 16 Paxinos, G., Franklin, K.B.J., The Mouse Brain in Stereotaxic Coordinates. 2nd ed., 2001, Academic Press, San Diego.
17. 17 Dickinson, A., Nicholas, D., Adams, C.D., The effect of the instrumental training contingency on susceptibility to reinforcer devaluation. Q J. Exp Psychol A 35 (1983), 35–51.
18. 18 Gourley, S.L., Swanson, A.M., Jacobs, A.M., Howell, J.L., Mo, M., Dileone, R.J., et al. Action control is mediated by prefrontal BDNF and glucocorticoid receptor binding. Proc Natl Acad Sci U S A 109 (2012), 20714–20719.
19. 19 Swanson, A.M., Shapiro, L.P., Whyte, A.J., Gourley, S.L., Glucocorticoid receptor regulation of action selection and prefrontal cortical dendritic spines. Commun Integr Biol, 6, 2013, e26068.
20. 20 Hinton, E.A., Wheeler, M.G., Gourley, S.L., Early-life cocaine interferes with BDNF-mediated behavioral plasticity. Learn Mem 21 (2014), 253–257.
21. 21 Gourley, S.L., Swanson, A.M., Koleske, A.J., Corticosteroid-induced neural remodeling predicts behavioral vulnerability and resilience. J Neurosci 33 (2013), 3107–3112.
22. 22 Peters, A., Kaiserman-Abramof, I.R., The small pyramidal neuron of the rat cerebral cortex. The perikaryon, dendrites and spines. Am J Anat 127 (1970), 321–355.
23. 23 Gourley, S.L., Lee, A.S., Howell, J.L., Pittenger, C., Taylor, J.R., Dissociable regulation of instrumental action within mouse prefrontal cortex. Eur J Neurosci 32 (2010), 1726–1734.
24. 24 Suzuki, W.A., Amaral, D.G., Cortical inputs to the CA1 field of the monkey hippocampus originate from the perirhinal and parahippocampal cortex but not from area TE. Neurosci Lett 115 (1990), 43–48.
25. 25 Van Hoesen, G., Pandya, D.N., Butters, N., Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. II. Frontal lobe afferents. Brain Res 95 (1975), 25–38.
26. 26 Schilman, E.A., Uylings, H.B., Galis-de Graaf, Y., Joel, D., Groenewegen, H.J., The orbital cortex in rats topographically projects to central parts of the caudate-putamen complex. Neurosci Lett 432 (2008), 40–45.
27. 27 Berendse, H.W., Galis-de Graaf, Y., Groenewegen, H.J., Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat. J Comp Neurol 316 (1992), 314–347.
28. 28 Oh, S.W., Harris, J.A., Ng, L., Winslow, B., Cain, N., Mihalas, S., et al. A mesoscale connectome of the mouse brain. Nature 508 (2014), 207–214.
29. 29 Matyas, F., Lee, J., Shin, H.S., Acsady, L., The fear circuit of the mouse forebrain: connections between the mediodorsal thalamus, frontal cortices and basolateral amygdala. Eur J Neurosci 39 (2014), 1810–1823.
30. 30 Dong H, et al. Mouse Connectome Project. Available at: http://www.mouseconnectome.org/. Accessed September 27, 2015.
31. 31 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 28 (2008), 1437–1448.
32. 32 Corbit, L.H., Balleine, B.W., The role of prelimbic cortex in instrumental conditioning. Behav Brain Res 146 (2003), 145–157.
33. 33 Altar, C.A., Cai, N., Bliven, T., Juhasz, M., Conner, J.M., Acheson, A.L., et al. Anterograde transport of brain-derived neurotrophic factor and its role in the brain. Nature 389 (1997), 856–860.
34. 34 Conner, J.M., Lauterborn, J.C., Yan, Q., Gall, C.M., Varon, S., Distribution of brain-derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: Evidence for anterograde axonal transport. J Neurosci 17 (1997), 2295–2313.
35. 35 Jang, S.W., Liu, X., Yepes, M., Shepherd, K.R., Miller, G.W., Liu, Y., et al. A selective TrkB agonist with potent neurotrophic activities by 7,8-dihydroxyflavone. Proc Natl Acad Sci U S A 107 (2010), 2687–2692.
36. 36 Cazorla, M., Premont, J., Mann, A., Girard, N., Kellendonk, C., Rognan, D., Identification of a low-molecular weight TrkB antagonist with anxiolytic and antidepressant activity in mice. J Clin Invest 121 (2011), 1846–1857.
37. 37 Graybeal, C., Feyder, M., Schulman, E., Saksida, L.M., Bussey, T.J., Brigman, J.L., et al. Paradoxical reversal learning enhancement by stress or prefrontal cortical damage: Rescue with BDNF. Nat Neurosci 14 (2011), 1507–1509.
38. 38 Hammond, L.J., The effect of contingency upon the appetitive conditioning of free-operant behavior. J Exp Anal Behav 34 (1980), 297–304.
39. 39 Panayi, M.C., Killcross, S., Orbitofrontal cortex inactivation impairs between- but not within-session Pavlovian extinction: An associative analysis. Neurobiol Learn Mem 108 (2014), 78–87.
40. 40 Andero, R., Heldt, S.A., Ye, K., Liu, X., Armario, A., Ressler, K.J., Effect of 7,8-dihydroxyflavone, a small-molecule TrkB agonist, on emotional learning. Am J Psychiatry 168 (2011), 163–172.
41. 41 Reichardt, L.F., Neurotrophin-regulated signalling pathways. Philos Trans R Soc Lond B Biol Sci 361 (2006), 1545–1564.
42. 42 Davis, M., The role of the amygdala in fear and anxiety. Annu Rev Neurosci 15 (1992), 353–375.
43. 43 Fanselow, M.S., LeDoux, J.E., Why we think plasticity underlying Pavlovian fear conditioning occurs in the basolateral amygdala. Neuron 23 (1999), 229–232.
44. 44 Groenewegen, H.J., Uylings, H.B., The prefrontal cortex and the integration of sensory, limbic and autonomic information. Prog Brain Res 126 (2000), 3–28.
45. 45 Barbas, H., Connections underlying the synthesis of cognition, memory, and emotion in primate prefrontal cortices. Brain Res Bull 52 (2000), 319–330.
46. 46 Balleine, B.W., O'Doherty, J.P., Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual action. Neuropsychopharmacology 35 (2010), 48–69.
47. 47 Gourley, S.L., Olevska, A., Gordon, J., Taylor, J.R., Cytoskeletal determinants of stimulus-response habits. J Neurosci 33 (2013), 11811–11816.
48. 48 Wellman, L.L., Gale, K., Malkova, L., GABAA-mediated inhibition of basolateral amygdala blocks reward devaluation in macaques. J Neurosci 25 (2005), 4577–4586.
49. 49 West, E.A., Forcelli, P.A., Murnen, A.T., McCue, D.L., Gale, K., Malkova, L., Transient inactivation of basolateral amygdala during selective satiation disrupts reinforcer devaluation in rats. Behav Neurosci 126 (2012), 563–574.
50. 50 Parkes, S.L., Balleine, B.W., Incentive memory: Evidence the basolateral amygdala encodes and the insular cortex retrieves outcome values to guide choice between goal-directed actions. J Neurosci 33 (2013), 8753–8763.
51. 51 Holland, P.C., Gallagher, M., Amygdala-frontal interactions and reward expectancy. Curr Opin Neurobiol 14 (2004), 148–155.
52. 52 Schoenbaum, G., Setlow, B., Saddoris, M.P., Gallagher, M., Encoding predicted outcome and acquired value in orbitofrontal cortex during cue sampling depends upon input from basolateral amygdala. Neuron 39 (2003), 855–867.
53. 53 Ghashghaei, H.T., Barbas, H., Pathways for emotion: Interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey. Neuroscience 115 (2002), 1261–1279.
54. 54 Li, C., Dabrowska, J., Hazra, R., Rainnie, D.G., Synergistic activation of dopamine D1 and TrkB receptors mediate gain control of synaptic plasticity in the basolateral amygdala. PLoS One, 6, 2011, e26065.
55. 55 Balkowiec, A., Katz, D.M., Cellular mechanisms regulating activity-dependent release of native brain-derived neurotrophic factor from hippocampal neurons. J Neurosci 22 (2002), 10399–10407.
56. 56 Gartner, A., Staiger, V., Neurotrophin secretion from hippocampal neurons evoked by long-term-potentiation-inducing electrical stimulation patterns. Proc Natl Acad Sci U S A 99 (2002), 6386–6391.
57. 57 Dong, S., Allen, J.A., Farrell, M., Roth, B.L., A chemical-genetic approach for precise spatio-temporal control of cellular signaling. Mol Biosyst 6 (2010), 1376–1380.
58. 58 Hearing, M.C., Miller, S.W., See, R.E., McGinty, J.F., Relapse to cocaine seeking increases activity-regulated gene expression differentially in the prefrontal cortex of abstinent rats. Psychopharmacology (Berl) 198 (2008), 77–91.
59. 59 Gourley, S.L., Kedves, A.T., Olausson, P., Taylor, J.R., A history of corticosterone exposure regulates fear extinction and cortical NR2B, GluR2/3, and BDNF. Neuropsychopharmacology 34 (2009), 707–716.
60. 60 Rosen G, Williams AG, Capra JA, Connolly MT, Cruz B, Lu L, et al. (2000): International Mouse Genome Conference. The Mouse Brain Library. Available at: http://www.Mbl.Org. Accessed May 2, 2011.