Vulnerability factors in anxiety: Strain and sex differences in the use of signals associated with non-threat during the acquisition and extinction of active-avoidance behavior

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 35, Issue 7, 2011, Pages 1659-1670

  Beck, Kevin D ^a,b   Jiao, Xilu ^b   Ricart, Thomas M ^b   Myers, Catherine E ^a,b   Minor, Thomas R ^b,c   Pang, Kevin C H ^a,b   Servatius, Richard J ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Avoidance; Behavioral inhibition; Classical conditioning; Instrumental learning; Safety; Sex differences

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY DISORDER; ARTICLE; AVOIDANCE BEHAVIOR; BEHAVIORAL SCIENCE; CONTROLLED STUDY; CORRELATIONAL STUDY; ESCAPE BEHAVIOR; EYELID REFLEX; FEMALE; INBRED STRAIN; MALE; NONHUMAN; OUTBRED STRAIN; RAT; RAT STRAIN; REINFORCEMENT; SEX DIFFERENCE; SIGNAL DETECTION; STATE DEPENDENT LEARNING; STIMULUS RESPONSE; STRAIN DIFFERENCE; VISUAL STIMULATION;

ANIMALS; ANXIETY; ANXIETY DISORDERS; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; BLINKING; CONDITIONING, CLASSICAL; CONDITIONING, OPERANT; EXTINCTION, PSYCHOLOGICAL; FEMALE; LEARNING; MALE; RATS; RATS, INBRED WKY; RATS, SPRAGUE-DAWLEY; RISK FACTORS; SEX FACTORS; SPECIES SPECIFICITY;

EID: 79961128130     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2011.05.002     Document Type: Article

References (63)

1. American Psychiatric Association Diagnostic and statistical manual of mental disorders 2000, American Psychiatric Association, Washington, DC.
2. Ballenger J.C., Davidson J.R., Lecrubier Y., Nutt D.J., Foa E.B., Kessler R.C., McFarlane A.C., Shalev A.Y. Consensus statement on posttraumatic stress disorder from the International Consensus Group on Depression and Anxiety. J Clin Psychiatry 2000, 61(Suppl. 5):60-66.
3. Baum A.E., Solberg L.C., Churchill G.A., Ahmadiyeh N., Takahashi J.S., Redei E.E. Test- and behavior-specific genetic factors affect WKY hypoactivity in tests of emotionality. Behav Brain Res 2006, 169:220-230.
4. Beck K.D., McLaughlin J., Bergen M.T., Cominski T.P., Moldow R.L., Servatius R.J. Facilitated acquisition of the classically conditioned eyeblink response in women taking oral contraceptives. Behav Pharmacol 2008, 19:821-828.
5. Beck K.D., Jiao X., Pang K.C., Servatius R.J. Vulnerability factors in anxiety determined through differences in active-avoidance behavior. Prog Neuropsychopharmacol Biol Psychiatry 2010, 34:852-860.
6. Berger D.F., Brush F.R. Rapid acquisition of discrete-trial lever-press avoidance: effects of signal-shock interval. J Exp Anal Behav 1975, 24:227-239.
7. Berger D.F., Starzec J.J. Contrasting lever-press avoidance behaviors of spontaneously hypertensive and normotensive rats (Rattus norvegicus). J Comp Psychol 1988, 102:279-286.
8. Berger D.F., Starzec J.J., Mason E.B. The relationship between plasma corticosterone levels and leverpress avoidance vs. escape behaviors in rats. Physiol Psychol 1981, 9:81-86.
9. Best M.R. Conditioned and latent inhibition in taste-aversion learning: clarifying the role of learned safety. J Exp Psychol Anim Behav Process 1975, 1:97-113.
10. Biederman J., Hirshfeld-Becker D.R., Rosenbaum J.F., Herot C., Friedman D., Snidman N., Kagan J., Faraone S.V. Further evidence of association between behavioral inhibition and social anxiety in children. Am J Psychiatry 2001, 158:1673-1679.
11. Brennan F.X., Beck K.D., Servatius R.J. Leverpress escape/avoidance conditioning in rats: safety signal length and avoidance performance. Integr Physiol Behav Sci 2003, 38:36-44.
12. Brennan F.X., Beck K.D., Servatius R.J. Proinflammatory cytokines differentially affect leverpress avoidance acquisition in rats. Behav Brain Res 2004, 153:351-355.
13. Breslau N., Kessler R.C., Chilcoat H.D., Schultz L.R., Davis G.C., Andreski P. Trauma and posttraumatic stress disorder in the community: the 1996 Detroit Area Survey of Trauma. Arch Gen Psychiatry 1998, 55:626-632.
14. Carter M.M., Hollon S.D., Carson R., Shelton R.C. Effects of a safe person on induced distress following a biological challenge in panic disorder with agoraphobia. J Abnorm Psychol 1995, 104:156-163.
15. Clements K.M., Saunders A.J., Robertson B.A., Wainwright P.E. Spontaneously hypertensive, Wistar Kyoto and Sprague-Dawley rats differ in their use of place and response strategies in the water radial arm maze. Neurobiol Learn Mem 2007, 87:285-294.
16. Dillow P.V., Myerson J., Slaughter L., Hurwitz H.M. Safety signals and the aquisition and extinction of lever-press discriminated avoidance in rats. Br J Psychol 1972, 63:583-591.
17. Ferguson S.A., Cada A.M. Spatial learning/memory and social and nonsocial behaviors in the spontaneously hypertensive, Wistar-Kyoto and Sprague-Dawley rat strains. Pharmacol Biochem Behav 2004, 77:583-594.
18. Gabriele A., Packard M.G. Evidence of a role for multiple memory systems in behavioral extinction. Neurobiol Learn Mem 2006, 85:289-299.
19. Grillon C., Falls W.A., Ameli R., Davis M. Safety signals and human anxiety: a fear-potentiated startle study. Anxiety 1994, 1:13-21.
20. Hirshfeld D.R., Rosenbaum J.F., Biederman J., Bolduc E.A., Faraone S.V., Snidman N., Reznick J.S., Kagan J. Stable behavioral inhibition and its association with anxiety disorder. J Am Acad Child Adolesc Psychiatry 1992, 31:103-111.
21. Hirshfeld-Becker D.R., Biederman J., Henin A., Faraone S.V., Davis S., Harrington K., Rosenbaum J.F. Behavioral inhibition in preschool children at risk is a specific predictor of middle childhood social anxiety: a five-year follow-up. J Dev Behav Pediatr 2007, 28:225-233.
22. Hoffman H.S., Fleshler M., Chorny H. Discriminated bar-press avoidance. J Exp Anal Behav 1961, 4:309-316.
23. Holland P.C. Transfer of negative occasion setting and conditioned inhibition across conditioned and unconditioned stimuli. J Exp Psychol Anim Behav Process 1989, 15:311-328.
24. Holloway J.L., Beck K.D., Servatius R.J. Facilitated acquisition of the classically conditioned eyeblink response in females is augmented in those taking oral contraceptives. Behav Brain Res 2011, 216:301-307.
25. Jiao X., Pang K.C., Beck K.D., Minor T.R., Servatius R.J. Avoidance perseveration during extinction training in Wistar-Kyoto rats: an interaction of innate vulnerability and stressor intensity. Behav Brain Res 2011, 221:98-107.
26. Kessler R.C., McGonagle K.A., Zhao S., Nelson C.B., Hughes M., Eshleman S., Wittchen H.U., Kendler K.S. Lifetime and 12-month prevalence of DSM-III-R psychiatric disorders in the United States. Results from the National Comorbidity Survey. Arch Gen Psychiatry 1994, 51:8-19.
27. Kessler R.C., Sonnega A., Bromet E., Hughes M., Nelson C.B. Posttraumatic stress disorder in the National Comorbidity Survey. Arch Gen Psychiatry 1995, 52:1048-1060.
28. Lovibond P.F., Davis N.R., O'Flaherty A.S. Protection from extinction in human fear conditioning. Behav Res Ther 2000, 38:967-983.
29. Lovinger D.M. Neurotransmitter roles in synaptic modulation, plasticity and learning in the dorsal striatum. Neuropharmacology 2010, 58:951-961.
30. Malkesman O., Braw Y., Zagoory-Sharon O., Golan O., Lavi-Avnon Y., Schroeder M., Overstreet D.H., Yadid G., Weller A. Reward and anxiety in genetic animal models of childhood depression. Behav Brain Res 2005, 164:1-10.
31. Milad M.R., Vidal-Gonzalez I., Quirk G.J. Electrical stimulation of medial prefrontal cortex reduces conditioned fear in a temporally specific manner. Behav Neurosci 2004, 118:389-394.
32. Myers, C.E., VanMeenen, K.M., McAuley, J.D., Beck, K.D., Pang, K.C.H., Servatius, R.J., accepted for publication. Behaviorally-inhibited temperament is associated with severity of PTSD symptoms and faster eyeblink conditioning in veterans. Stress.
33. Novick A., Yaroslavsky I., Tejani-Butt S. Strain differences in the expression of dopamine D1 receptors in Wistar-Kyoto (WKY) and Wistar rats. Life Sci 2008, 83:74-78.
34. Packard M.G. Anxiety, cognition, and habit: a multiple memory systems perspective. Brain Res 2009, 1293:121-128.
35. Packard M.G., Gabriele A. Peripheral anxiogenic drug injections differentially affect cognitive and habit memory: role of basolateral amygdala. Neuroscience 2009, 164:457-462.
36. Pare W.P. Investigatory behavior of a novel conspecific by Wistar Kyoto, Wistar and Sprague-Dawley rats. Brain Res Bull 2000, 53:759-765.
37. Poldrack R.A., Packard M.G. Competition among multiple memory systems: converging evidence from animal and human brain studies. Neuropsychologia 2003, 41:245-251.
38. Quirk G.J., Likhtik E., Pelletier J.G., Pare D. Stimulation of medial prefrontal cortex decreases the responsiveness of central amygdala output neurons. J Neurosci 2003, 23:8800-8807.
39. Rachman S. Agoraphobia: a safety-signal perspective. Behav Res Ther 1984, 22:59-70.
40. Rescorla R.A. Conditioned inhibition of fear resulting from negative CS-US contingencies. J Comp Physiol Psychol 1969, 67:504-509.
41. Ricart T.M., De Niear M.A., Jiao X., Pang K.C., Beck K.D., Servatius R.J. Deficient proactive interference of eyeblink conditioning in Wistar-Kyoto rats. Behav Brain Res 2011, 216:59-65.
42. Ricart T.M., Jiao X., Pang K.C., Beck K.D., Servatius R.J. Classical and instrumental conditioning of eyeblink responses in Wistar-Kyoto and Sprague-Dawley rats. Behav Brain Res 2011, 216:414-418.
43. Rosenbaum J.F., Biederman J., Hirshfeld D.R., Bolduc E.A., Chaloff J. Behavioral inhibition in children: a possible precursor to panic disorder or social phobia. J Clin Psychiatry 1991, 52:5-9. Suppl.
44. Rosenbaum J.F., Biederman J., Hirshfeld D.R., Bolduc E.A., Faraone S.V., Kagan J., Snidman N., Reznick J.S. Further evidence of an association between behavioral inhibition and anxiety disorders: results from a family study of children from a non-clinical sample. J Psychiatr Res 1991, 25:49-65.
45. Rosenbaum J.F., Biederman J., Bolduc-Murphy E.A., Faraone S.V., Chaloff J., Hirshfeld D.R., Kagan J. Behavioral inhibition in childhood: a risk factor for anxiety disorders. Harv Rev Psychiatry 1993, 1:2-16.
46. Santini E., Ge H., Ren K., Pena de O.S., Quirk G.J. Consolidation of fear extinction requires protein synthesis in the medial prefrontal cortex. J Neurosci 2004, 24:5704-5710.
47. Schmajuk N.A., Lamoureux J.A., Holland P.C. Occasion setting: a neural network approach. Psychol Rev 1998, 105:3-32.
48. Schmidt N.B., Telch M.J. Role of fear of fear and safety information in moderating the effects of voluntary hyperventilation. Behav Ther 1994, 25:197-208.
49. Schmidt N.B., Richey J.A., Maner J.K., Woolaway-Bickel K. Differential effects of safety in extinction of anxious responding to a CO2 challenge in patients with panic disorder. J Abnorm Psychol 2006, 115:341-350.
50. Sehlmeyer C., Dannlowski U., Schoning S., Kugel H., Pyka M., Pfleiderer B., Zwitserlood P., Schiffbauer H., Heindel W., Arolt V., Konrad C. Neural correlates of trait anxiety in fear extinction. Psychol Med 2011, 41:789-798.
51. Servatius R.J. Eyeblink conditioning in the freely moving rat: square-wave stimulation as the unconditioned stimulus. J Neurosci Methods 2000, 102:35-42.
52. Servatius R.J., Beck K.D. Facilitated acquisition of the classically conditioned eyeblink response in male rats after systemic IL-1beta. Integr Physiol Behav Sci 2003, 38:169-178.
53. Servatius R.J., Beck K.D., Moldow R.L., Salameh G., Tumminello T.P., Short K.R. A stress-induced anxious state in male rats: corticotropin-releasing hormone induces persistent changes in associative learning and startle reactivity. Biol Psychiatry 2005, 57:865-872.
54. Servatius R.J., Jiao X., Beck K.D., Pang K.C., Minor T.R. Rapid avoidance acquisition in Wistar-Kyoto rats. Behav Brain Res 2008, 192:191-197.
55. Shors T.J., Weiss C., Thompson R.F. Stress-induced facilitation of classical conditioning. Science 1992, 257:537-539.
56. Shors T.J., Lewczyk C., Pacynski M., Mathew P.R., Pickett J. Stages of estrous mediate the stress-induced impairment of associative learning in the female rat. Neuroreport 1998, 9:419-423.
57. Sidman M., Boren J.J. A comparison of two types of warning stimulus in an avoidance situation. J Comp Physiol Psychol 1957, 50:282-287.
58. Sierra-Mercado D., Corcoran K.A., Lebron-Milad K., Quirk G.J. Inactivation of the ventromedial prefrontal cortex reduces expression of conditioned fear and impairs subsequent recall of extinction. Eur J Neurosci 2006, 24:1751-1758.
59. Volkow N.D., Chang L., Wang G.J., Fowler J.S., Ding Y.S., Sedler M., Logan J., Franceschi D., Gatley J., Hitzemann R., Gifford A., Wong C., Pappas N. Low level of brain dopamine D2 receptors in methamphetamine abusers: association with metabolism in the orbitofrontal cortex. Am J Psychiatry 2001, 158:2015-2021.
60. Wittchen H.U., Zhao S., Kessler R.C., Eaton W.W. DSM-III-R generalized anxiety disorder in the National Comorbidity Survey. Arch Gen Psychiatry 1994, 51:355-364.
61. Wittchen H.U., Stein M.B., Kessler R.C. Social fears and social phobia in a community sample of adolescents and young adults: prevalence, risk factors and co-morbidity. Psychol Med 1999, 29:309-323.
62. Wood G.E., Shors T.J. Stress facilitates classical conditioning in males, but impairs classical conditioning in females through activational effects of ovarian hormones. Proc Natl Acad Sci USA 1998, 95:4066-4071.
63. Yaroslavsky I., Colletti M., Jiao X., Tejani-Butt S. Strain differences in the distribution of dopamine (DA-2 and DA-3) receptor sites in rat brain. Life Sci 2006, 79:772-776.