Anxiety evokes hypofrontality and disrupts rule-relevant encoding by dorsomedial prefrontal cortex neurons

Journal of Neuroscience

Volumn 36, Issue 11, 2016, Pages 3322-3335

  Park, Junchol ^a   Wood, Jesse ^a   Bondi, Corina ^a,b   Arco, Alberto Del ^c   Moghaddam, Bita ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MISSISSIPPI   (United States)

Author keywords

Addiction; Decision making; Dopamine; Schizophrenia; Stress

Indexed keywords

N METHYL BETA CARBOLINE 3 CARBOXAMIDE; 4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; CARBOLINE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CONTROLLED STUDY; DORSOMEDIAL PREFRONTAL CORTEX; ELEVATED PLUS MAZE TEST; FIRING RATE; MALE; NONHUMAN; ORBITAL CORTEX; PRIORITY JOURNAL; RAT; RECEIVER OPERATING CHARACTERISTIC; ACTION POTENTIAL; ANIMAL; ATTENTION; DISEASE MODEL; DRUG EFFECTS; MAZE TEST; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PREFRONTAL CORTEX; SPRAGUE DAWLEY RAT; STATISTICAL MODEL; WAKEFULNESS;

ACTION POTENTIALS; ANIMALS; ANXIETY; ATTENTION; CARBOLINES; DISEASE MODELS, ANIMAL; GABA ANTAGONISTS; LINEAR MODELS; MALE; MAZE LEARNING; NEURONS; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; ROC CURVE; WAKEFULNESS;

EID: 84961266477     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4250-15.2016     Document Type: Article

References (60)

1. Adhikari A (2014) Distributed circuits underlying anxiety. Front Behav Neurosci 8:112. CrossRef Medline
2. Adhikari A, Topiwala MA, Gordon JA (2010) Synchronized activity between the ventral hippocampus and the medial prefrontal cortex during anxiety. Neuron 65:257–269. CrossRef Medline
3. Adhikari A, Topiwala MA, Gordon JA (2011) Single units in the medial prefrontal cortex with anxiety-related firing patterns are preferentially influenced by ventral hippocampal activity. Neuron 71:898–910. CrossRef Medline
4. Arnsten AF (2000) Stress impairs prefrontal cortical function in rats and monkeys: role of dopamine D1 and norepinephrine alpha-1 receptor mechanisms. Prog Brain Res 126:183–192. CrossRef Medline
5. Arnsten AF (2009) Stress signalling pathways that impair prefrontal cortex structure and function. Nat Rev Neurosci 10:410–422. CrossRef Medline
6. Atack JR, Hutson PH, Collinson N, Marshall G, Bentley G, Moyes C, Cook SM, Collins I, Wafford K, McKernan RM, Dawson GR (2005) Anxiogenic properties of an inverse agonist selective for alpha3 subunitcontaining GABA A receptors. Br J Pharmacol 144:357–366. CrossRef Medline
7. Bishop SJ (2007) Neurocognitive mechanisms of anxiety: an integrative account. Trends Cogn Sci 11:307–316. CrossRef Medline
8. Bissonette GB, Martins GJ, Franz TM, Harper ES, Schoenbaum G, Powell EM (2008) Double dissociation of the effects of medial and orbital prefrontal cortical lesions on attentional and affective shifts in mice. J Neurosci 28:11124–11130. CrossRef Medline
9. Bradberry CW, Lory JD, Roth RH (1991) The anxiogenic beta-carboline FG 7142 selectively increases dopamine release in rat prefrontal cortex as measured by microdialysis. J Neurochem 56:748–752. CrossRef Medline
10. Burgos-Robles A, Vidal-Gonzalez I, Quirk GJ (2009) Sustained conditioned responses in prelimbic prefrontal neurons are correlated with fear expression and extinction failure. J Neurosci 29:8474–8482. CrossRef Medline
11. Butts KA, Floresco SB, Phillips AG (2013) Acute stress impairs set-shifting but not reversal learning. Behav Brain Res 252:222–229. CrossRef Medline
12. Calhoon GG, Tye KM (2015) Resolving the neural circuits of anxiety. Nat Neurosci 18:1394–1404. CrossRef Medline
13. Cha J, Carlson JM, Dedora DJ, Greenberg T, Proudfit GH, Mujica-Parodi LR (2014) Hyper-reactive human ventral tegmental area and aberrant mesocorticolimbic connectivity in overgeneralization of fear in generalized anxiety disorder. J Neurosci 34:5855–5860. CrossRef Medline
14. Cole BJ, Hillmann M, Seidelmann D, Klewer M, Jones GH (1995) Effects of benzodiazepine receptor partial inverse agonists in the elevated plus maze test of anxiety in the rat. Psychopharmacology 121:118–126. CrossRef Medline
15. Darrah JM, Stefani MR, Moghaddam B (2008) Interaction of N-methyl-Daspartate and group 5 metabotropic glutamate receptors on behavioral flexibility using a novel operant set-shift paradigm. Behav Pharmacol 19:225–234. CrossRef Medline
16. Dias R, Robbins TW, Roberts AC (1997) Dissociable forms of inhibitory control within prefrontal cortex with an analog of the Wisconsin Card Sort Test: restriction to novel situations and independence from “online” processing. J Neurosci 17:9285–9297. Medline
17. Dorow R (1987) FG 7142 and its anxiety-inducing effects in humans. Br J Clin Pharmacol 23:781–782. Medline
18. Durstewitz D, Vittoz NM, Floresco SB, Seamans JK (2010) Abrupt transitions between prefrontal neural ensemble states accompany behavioral transitions during rule learning. Neuron 66:438–448. CrossRef Medline
19. Evans AK, Lowry CA (2007) Pharmacology of the beta-carboline FG-7142, a partial inverse agonist at the benzodiazepine allosteric site of the GABA A receptor: neurochemical, neurophysiological, and behavioral effects. CNS Drug Rev 13:475–501. CrossRef Medline
20. Eysenck MW, Derakshan N, Santos R, Calvo MG (2007) Anxiety and cognitive performance: attentional control theory. Emotion 7:336–353. CrossRef Medline
21. Floresco SB, Block AE, Tse MT (2008) Inactivation of the medial prefrontal cortex of the rat impairs strategy set-shifting, but not reversal learning, using a novel, automated procedure. Behav Brain Res 190:85–96. CrossRef Medline
22. Gamo NJ, Lur G, Higley MJ, Wang M, Paspalas CD, Vijayraghavan S, Yang Y, Ramos BP, Peng K, Kata A, Boven L, Lin F, Roman L, Lee D, Arnsten AF (2015) Stress impairs prefrontal cortical function via D1 dopamine receptor interactions with hyperpolarization-activated cyclic nucleotidegated channels. Biol Psychiatry 78:860–870. CrossRef Medline
23. Goldstein LE, Rasmusson AM, Bunney BS, Roth RH (1996) Role of the amygdala in the coordination of behavioral, neuroendocrine, and prefrontal cortical monoamine responses to psychological stress in the rat. J Neurosci 16:4787–4798. Medline
24. Gorelova N, Seamans JK, Yang CR (2002) Mechanisms of dopamine activation of fast-spiking interneurons that exert inhibition in rat prefrontal cortex. J Neurophysiol 88:3150–3166. CrossRef Medline
25. Gunaydin LA, Grosenick L, Finkelstein JC, Kauvar IV, Fenno LE, Adhikari A, Lammel S, Mirzabekov JJ, Airan RD, Zalocusky KA, Tye KM, Anikeeva P, Malenka RC, Deisseroth K (2014) Natural neural projection dynamics underlying social behavior. Cell 157:1535–1551. CrossRef Medline
26. Hains AB, Arnsten AF (2008) Molecular mechanisms of stress-induced prefrontal cortical impairment: implications for mental illness. Learn Mem 15:551–564. CrossRef Medline
27. Hamilton JP, Chen MC, Waugh CE, Joormann J, Gotlib IH (2015) Distinctive and common neural underpinnings of major depression, social anxiety, and their comorbidity. Soc Cogn Affect Neurosci 10:552–560. CrossRef Medline
28. Homayoun H, Moghaddam B (2007) NMDA receptor hypofunction produces opposite effects on prefrontal cortex interneurons and pyramidal neurons. J Neurosci 27:11496–11500. CrossRef Medline
29. Lammel S, Lim BK, Ran C, Huang KW, Betley MJ, Tye KM, Deisseroth K, Malenka RC (2012) Input-specific control of reward and aversion in the ventral tegmental area. Nature 491:212–217. CrossRef Medline
30. Lee D (2013) Decision making: from neuroscience to psychiatry. Neuron 78:233–248. CrossRef Medline
31. Likhtik E, Stujenske JM, Topiwala MA, Harris AZ, Gordon JA (2014) Prefrontal entrainment of amygdala activity signals safety in learned fear and innate anxiety. Nat Neurosci 17:106–113. CrossRef Medline
32. Lüthi A, Lüscher C (2014) Pathological circuit function underlying addiction and anxiety disorders. Nat Neurosci 17:1635–1643. CrossRef Medline
33. McAlonan K, Brown VJ (2003) Orbital prefrontal cortex mediates reversal learning and not attentional set-shifting in the rat. Behav Brain Res 146: 97–103. CrossRef Medline
34. Meyers EM, Qi XL, Constantinidis C (2012) Incorporation of new information into prefrontal cortical activity after learning working memory tasks. Proc Natl Acad Sci U S A 109:4651–4656. CrossRef Medline
35. Mikkelsen JD, Søderman A, Kiss A, Mirza N (2005) Effects of benzodiazepines receptor agonists on the hypothalamic-pituitary-adrenocortical axis. Eur J Pharmacol 519:223–230. CrossRef Medline
36. Milad MR, Quirk GJ (2002) Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 420:70–74. CrossRef Medline
37. Milad MR, Quirk GJ (2012) Fear extinction as a model for translational neuroscience: ten years of progress. Annu Rev Psychol 63:129–151. CrossRef Medline
38. Murphy BL, Arnsten AF, Goldman-Rakic PS, Roth RH (1996a) Increased dopamine turnover in the prefrontal cortex impairs spatial working memory performance in rats and monkeys. Proc Natl Acad Sci U S A 93:1325–1329. CrossRef Medline
39. Murphy BL, Arnsten AF, Jentsch JD, Roth RH (1996b) Dopamine and spatial working memory in rats and monkeys: pharmacological reversal of stress-induced impairment. J Neurosci 16:7768–7775. Medline
40. Ninan PT, Insel TM, Cohen RM, Cook JM, Skolnick P, Paul SM (1982) Benzodiazepine receptor-mediated experimental “anxiety” in primates. Science 218:1332–1334. CrossRef Medline
41. Ouimet AJ, Gawronski B, Dozois DJ (2009) Cognitive vulnerability to anxiety: a review and an integrative model. Clin Psychol Rev 29:459–470. CrossRef Medline
42. Owens DG, Miller P, Lawrie SM, Johnstone EC (2005) Pathogenesis of schizophrenia: a psychopathological perspective. Br J Psychiatry 186: 386–393. CrossRef Medline
43. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. San Diego: Academic.
44. Pehrson AL, Bondi CO, Totah NK, Moghaddam B (2013) The influence of NMDA and GABA(A) receptors and glutamic acid decarboxylase (GAD) activity on attention. Psychopharmacology 225:31–39. CrossRef Medline
45. Pellow S, File SE (1986) Anxiolytic and anxiogenic drug effects on exploratory activity in an elevated plus-maze: a novel test of anxiety in the rat. Pharmacol Biochem Behav 24:525–529. CrossRef Medline
46. Phelps EA, Delgado MR, Nearing KI, LeDoux JE (2004) Extinction learning in humans: role of the amygdala and vmPFC. Neuron 43:897–905. CrossRef Medline
47. Purcell R, Maruff P, Kyrios M, Pantelis C (1998) Cognitive deficits in obsessive-compulsive disorder on tests of frontal-striatal function. Biol Psychiatry 43:348–357. CrossRef Medline
48. Reinhard JF Jr, Bannon MJ, Roth RH (1982) Acceleration by stress of dopamine synthesis and metabolism in prefrontal cortex: antagonism by diazepam. Naunyn Schmiedebergs Arch Pharmacol 318:374–377. CrossRef Medline
49. Robinson OJ, Vytal K, Cornwell BR, Grillon C (2013) The impact of anxiety upon cognition: perspectives from human threat of shock studies. Front Hum Neurosci 7:203. CrossRef Medline
50. Ruglass LM, Lopez-Castro T, Cheref S, Papini S, Hien DA (2014) At the crossroads: the intersection of substance use disorders, anxiety disorders, and posttraumatic stress disorder. Curr Psychiatr Rep 16:505. CrossRef Medline
51. Schoenbaum G, Roesch MR, Stalnaker TA, Takahashi YK (2009) A new perspective on the role of the orbitofrontal cortex in adaptive behaviour. Nat Rev Neurosci 10:885–892. CrossRef Medline
52. Seamans JK, Gorelova N, Durstewitz D, Yang CR (2001) Bidirectional dopamine modulation of GABAergic inhibition in prefrontal cortical pyramidal neurons. J Neurosci 21:3628–3638. Medline
53. Sesack SR, Bunney BS (1989) Pharmacological characterization of the receptor mediating electrophysiological responses to dopamine in the rat medial prefrontal cortex: a microiontophoretic study. J Pharmacol Exp Ther 248:1323–1333. Medline
54. Shin LM, Whalen PJ, Pitman RK, Bush G, Macklin ML, Lasko NB, Orr SP, McInerney SC, Rauch SL (2001) An fMRI study of anterior cingulate function in posttraumatic stress disorder. Biol Psychiatry 50:932–942. CrossRef Medline
55. Solomon M, Ozonoff S, Carter C, Caplan R (2008) Formal thought disorder and the autism spectrum: relationship with symptoms, executive control, and anxiety. J Autism Dev Disord 38:1474–1484. CrossRef Medline
56. Sotres-Bayon F, Bush DE, LeDoux JE (2004) Emotional perseveration: an update on prefrontal-amygdala interactions in fear extinction. Learn Mem 11:525–535. CrossRef Medline
57. Stefani MR, Moghaddam B (2005) Systemic and prefrontal cortical NMDA receptor blockade differentially affect discrimination learning and setshift ability in rats. Behav Neurosci 119:420–428. CrossRef Medline
58. Strait CE, Blanchard TC, Hayden BY (2014) Reward value comparison via mutual inhibition in ventromedial prefrontal cortex. Neuron 82:1357–1366. CrossRef Medline
59. Sul JH, Kim H, Huh N, Lee D, Jung MW (2010) Distinct roles of rodent orbitofrontal and medial prefrontal cortex in decision making. Neuron 66:449–460. CrossRef Medline
60. White JA, Banks MI, Pearce RA, Kopell NJ (2000) Networks of interneurons with fast and slow gamma-aminobutyric acid type A (GABAA) kinetics provide substrate for mixed gamma-theta rhythm. Proc Natl Acad Sci U S A 97:8128–8133. CrossRef Medline