Lesions of the paraventricular nucleus of the thalamus differentially affect sign- and goal-tracking conditioned responses

European Journal of Neuroscience

Volumn 42, Issue 7, 2015, Pages 2478-2488

  Haight, Joshua L ^a   Fraser, Kurt M ^a   Akil, Huda ^b,c   Flagel, Shelly B ^a,b,c  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Incentive salience; Motivation; Paraventricular nucleus of the thalamus; Pavlovian conditioning; Rats

Indexed keywords

ADULT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BRAIN DAMAGE; CONDITIONING; CONTROLLED STUDY; EXCITOTOXICITY; EYE TRACKING; HIPPOCAMPUS; LOCOMOTION; MALE; MOTIVATION; NEUROANATOMY; NONHUMAN; PARAVENTRICULAR THALAMIC NUCLEUS; PHENOTYPE; PRIORITY JOURNAL; RAT; REWARD; SUBICULUM; TRAINING; ANIMAL; ASSOCIATION; CONDITIONED REFLEX; DISEASE MODEL; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; BEHAVIOR, ANIMAL; CONDITIONING, CLASSICAL; CUES; DISEASE MODELS, ANIMAL; MALE; MOTIVATION; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; RATS; RATS, SPRAGUE-DAWLEY; REWARD;

EID: 84942986306     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.13031     Document Type: Article

References (50)

1. Balleine, B.W. & Dickinson, A. (1998) Goal-directed instrumental action: contingency and incentive learning and their cortical substrates. Neuropharmacology, 37, 407-419.
2. Browning, J.R., Jansen, H.T. & Sorg, B.A. (2014) Inactivation of the paraventricular thalamus abolishes the expression of cocaine conditioned place preference in rats. Drug Alcohol Depen., 134, 387-390.
3. Choi, D.L., Davis, J.F., Fitzgerald, M.E. & Benoit, S.C. (2010) The role of orexin-A in food motivation, reward-based feeding behavior and food-induced neuronal activation in rats. Neuroscience, 167, 11-20.
4. Dayas, C.V., McGranahan, T.M., Martin-Fardon, R. & Weiss, F. (2008) Stimuli linked to ethanol availability activate hypothalamic CART and orexin neurons in a reinstatement model of relapse. Biol. Psychiat., 63, 152-157.
5. Fitzpatrick, C.J., Gopalakrishnan, S., Cogan, E.S., Yager, L.M., Meyer, P.J., Lovic, V., Saunders, B.T., Parker, C.C., Gonzales, N.M., Aryee, E., Flagel, S.B., Palmer, A.A., Robinson, T.E. & Morrow, J.D. (2013) Variation in the form of Pavlovian conditioned approach behavior among outbred male Sprague-Dawley rats from different vendors and colonies: sign-tracking vs. goal-tracking. PLoS One, 8, e75042.
6. Flagel, S.B., Watson, S.J., Robinson, T.E. & Akil, H. (2007) Individual differences in the propensity to approach signals vs goals promote different adaptations in the dopamine system of rats. Psychopharmacology, 191, 599-607.
7. Flagel, S.B., Watson, S.J., Akil, H. & Robinson, T.E. (2008) Individual differences in the attribution of incentive salience to a reward-related cue: influence on cocaine sensitization. Behav. Brain Res., 186, 48-56.
8. Flagel, S.B., Akil, H. & Robinson, T.E. (2009) Individual differences in the attribution of incentive salience to reward-related cues: implications for addiction. Neuropharmacology, 56(Suppl 1), 139-148.
9. Flagel, S.B., Robinson, T.E., Clark, J.J., Clinton, S.M., Watson, S.J., Seeman, P., Phillips, P.E. & Akil, H. (2010) An animal model of genetic vulnerability to behavioral disinhibition and responsiveness to reward-related cues: implications for addiction. Neuropsychopharmacology, 35, 388-400.
10. Flagel, S.B., Cameron, C.M., Pickup, K.N., Watson, S.J., Akil, H. & Robinson, T.E. (2011a) A food predictive cue must be attributed with incentive salience for it to induce c-fos mRNA expression in cortico-striatal-thalamic brain regions. Neuroscience, 196, 80-96.
11. Flagel, S.B., Clark, J.J., Robinson, T.E., Mayo, L., Czuj, A., Willuhn, I., Akers, C.A., Clinton, S.M., Phillips, P.E. & Akil, H. (2011b) A selective role for dopamine in stimulus-reward learning. Nature, 469, 53-57.
12. Flagel, S.B., Waselus, M., Clinton, S.M., Watson, S.J. & Akil, H. (2014) Antecedents and consequences of drug abuse in rats selectively bred for high and low response to novelty. Neuropharmacology, 76(Part B), 425-436.
13. Haight, J.L. & Flagel, S.B. (2014) A potential role for the paraventricular nucleus of the thalamus in mediating individual variation in Pavlovian conditioned responses. Front. Behav. Neurosci., 8, 79.
14. Hamlin, A.S., Clemens, K.J., Choi, E.A. & McNally, G.P. (2009) Paraventricular thalamus mediates context-induced reinstatement (renewal) of extinguished reward seeking. Eur. J. Neurosci., 29, 802-812.
15. Igelstrom, K.M., Herbison, A.E. & Hyland, B.I. (2010) Enhanced c-Fos expression in superior colliculus, paraventricular thalamus and septum during learning of cue-reward association. Neuroscience, 168, 706-714.
16. James, M.H. & Dayas, C.V. (2013) What about me...? The PVT: a role for the paraventricular thalamus (PVT) in drug-seeking behaviour. Front. Behav. Neurosci., 7, 18.
17. James, M.H., Charnley, J.L., Flynn, J.R., Smith, D.W. & Dayas, C.V. (2011) Propensity to 'relapse' following exposure to cocaine cues is associated with the recruitment of specific thalamic and epithalamic nuclei. Neuroscience, 199, 235-242.
18. Johnson, Z.V., Revis, A.A., Burdick, M.A. & Rhodes, J.S. (2010) A similar pattern of neuronal Fos activation in 10 brain regions following exposure to reward- or aversion-associated contextual cues in mice. Physiol. Behav., 99, 412-418.
19. Jones, M.W., Kilpatrick, I.C. & Phillipson, O.T. (1989) Regulation of dopamine function in the nucleus accumbens of the rat by the thalamic paraventricular nucleus and adjacent midline nuclei. Exp. Brain Res., 76, 572-580.
20. Jonkman, S., Mar, A.C., Dickinson, A., Robbins, T.W. & Everitt, B.J. (2009) The rat prelimbic cortex mediates inhibitory response control but not the consolidation of instrumental learning. Behav. Neurosci., 123, 875-885.
21. Kelley, A.E., Baldo, B.A. & Pratt, W.E. (2005) A proposed hypothalamic-thalamic-striatal axis for the integration of energy balance, arousal, and food reward. J. Comp. Neurol., 493, 72-85.
22. Kirouac, G.J., Parsons, M.P. & Li, S. (2005) Orexin (hypocretin) innervation of the paraventricular nucleus of the thalamus. Brain Res., 1059, 179-188.
23. Kober, H., Mende-Siedlecki, P., Kross, E.F., Weber, J., Mischel, W., Hart, C.L. & Ochsner, K.N. (2010) Prefrontal-striatal pathway underlies cognitive regulation of craving. Proc. Natl. Acad. Sci. USA, 107, 14811-14816.
24. Lasseter, H.C., Xie, X., Ramirez, D.R. & Fuchs, R.A. (2010) Sub-region specific contribution of the ventral hippocampus to drug context-induced reinstatement of cocaine-seeking behavior in rats. Neuroscience, 171, 830-839.
25. Li, S. & Kirouac, G.J. (2012) Sources of inputs to the anterior and posterior aspects of the paraventricular nucleus of the thalamus. Brain Struct. Funct., 217, 257-273.
26. Li, S., Shi, Y. & Kirouac, G.J. (2014) The hypothalamus and periaqueductal gray are the sources of dopamine fibers in the paraventricular nucleus of the thalamus in the rat. Front. Neuroanat., 8, 136.
27. Mahler, S.V., Smith, R.J., Moorman, D.E., Sartor, G.C. & Aston-Jones, G. (2012) Multiple roles for orexin/hypocretin in addiction. Prog. Brain Res., 198, 79-121.
28. Marchant, N.J., Furlong, T.M. & McNally, G.P. (2010) Medial dorsal hypothalamus mediates the inhibition of reward seeking after extinction. J. Neurosci., 30, 14102-14115.
29. Marquis, J.-P., Killcross, S. & Haddon, J.E. (2007) Inactivation of the prelimbic, but not infralimbic, prefrontal cortex impairs the contextual control of response conflict in rats. Eur. J. Neurosci., 25, 559-566.
30. Martin-Fardon, R. & Boutrel, B. (2012) Orexin/hypocretin (Orx/Hcrt) transmission and drug-seeking behavior: is the paraventricular nucleus of the thalamus (PVT) part of the drug seeking circuitry? Front. Behav. Neurosci., 6, 75.
31. Meyer, P.J., Lovic, V., Saunders, B.T., Yager, L.M., Flagel, S.B., Morrow, J.D. & Robinson, T.E. (2012) Quantifying individual variation in the propensity to attribute incentive salience to reward cues. PLoS One, 7, e38987.
32. Mihindou, C., Guillem, K., Navailles, S., Vouillac, C. & Ahmed, S.H. (2013) Discriminative inhibitory control of cocaine seeking involves the prelimbic prefrontal cortex. Biol. Psychiat., 73, 271-279.
33. Parsons, M.P., Li, S. & Kirouac, G.J. (2006) The paraventricular nucleus of the thalamus as an interface between the orexin and CART peptides and the shell of the nucleus accumbens. Synapse, 59, 480-490.
34. Parsons, M.P., Li, S. & Kirouac, G.J. (2007) Functional and anatomical connection between the paraventricular nucleus of the thalamus and dopamine fibers of the nucleus accumbens. J. Comp. Neurol., 500, 1050-1063.
35. Pierce, R.C. & Kalivas, P.W. (1997) A circuitry model of the expression of behavioral sensitization to amphetamine-like psychostimulants. Brain Res. Rev., 25, 192-216.
36. Pierce, R.C., Reeder, D.C., Hicks, J., Morgan, Z.R. & Kalivas, P.W. (1997) Ibotenic acid lesions of the dorsal prefrontal cortex disrupt the expression of behavioral sensitization to cocaine. Neuroscience, 82, 1103-1114.
37. Robinson, T.E. & Flagel, S.B. (2009) Dissociating the predictive and incentive motivational properties of reward-related cues through the study of individual differences. Biol. Psychiat., 65, 869-873.
38. Saunders, B.T. & Robinson, T.E. (2012) The role of dopamine in the accumbens core in the expression of Pavlovian-conditioned responses. Eur. J. Neurosci., 36, 2521-2532.
39. Saunders, B.T., O'Donnell, E.G., Aurbach, E.L. & Robinson, T.E. (2014) A cocaine context renews drug seeking preferentially in a subset of individuals. Neuropsychopharmacology, 39, 2816-2823.
40. Schiltz, C., Kelley, A. & Landry, C. (2005a) Exposure to cues associated with palatable food increases immediate-early gene (IEG) mRNA and proenkephalin (PENK) premRNA expression in the rat brain. Neuropsychopharmacology, 30, S213.
41. Schiltz, C.A., Kelley, A.E. & Landry, C.F. (2005b) Contextual cues associated with nicotine administration increase arc mRNA expression in corticolimbic areas of the rat brain. Eur. J. Neurosci., 21, 1703-1711.
42. Schiltz, C., Bremer, Q., Landry, C. & Kelley, A. (2007) Food-associated cues alter forebrain functional connectivity as assessed with immediate early gene and proenkephalin expression. BMC Biol., 5, 16.
43. Stead, J.H., Clinton, S., Neal, C., Schneider, J., Jama, A., Miller, S., Vazquez, D., Watson, S. & Akil, H. (2006) Selective breeding for divergence in novelty-seeking traits: heritability and enrichment in spontaneous anxiety-related behaviors. Behav. Genet., 36, 697-712.
44. Sun, W. & Rebec, G.V. (2003) Lidocaine inactivation of ventral subiculum attenuates cocaine-seeking behavior in rats. J. Neurosci., 23, 10258-10264.
45. Verbeke, G. & Molenberghs, G. (2000) Linear Mixed Models for Longitudinal Data. Springer, New York.
46. Vertes, R.P. & Hoover, W.B. (2008) Projections of the paraventricular and paratenial nuclei of the dorsal midline thalamus in the rat. J. Comp. Neurol., 508, 212-237.
47. Wedzony, K., Koros, E., Czyrak, A., Chocyk, A., Czepiel, K., Fijal, K., Mackowiak, M., Rogowski, A., Kostowski, W. & Bienkowski, P. (2003) Different pattern of brain c-Fos expression following re-exposure to ethanol or sucrose self-administration environment. N.-S. Arch. Pharmacol., 368, 331-341.
48. Willcocks, A.L. & McNally, G.P. (2013) The role of medial prefrontal cortex in extinction and reinstatement of alcohol-seeking in rats. Eur. J. Neurosci., 37, 259-268.
49. Yager, L.M., Pitchers, K.K., Flagel, S.B. & Robinson, T.E. (2014) Individual variation in the motivational and neurobiological effects of an opioid cue. Neuropsychopharmacology, 40, 1269-1277.
50. Young, C.D. & Deutch, A.Y. (1998) The effects of thalamic paraventricular nucleus lesions on cocaine-induced locomotor activity and sensitization. Pharmacol. Biochem. Be., 60, 753-758.