Sign and goal tracker rats process differently the incentive salience of a conditioned stimulus
Autoři:
Almudena Serrano-Barroso aff001; Juan Pedro Vargas aff001; Estrella Diaz aff001; Patricio O’Donnell aff002; Juan Carlos López aff001
Působiště autorů:
Departamento de Psicología Experimental, Universidad de Sevilla, Seville, Spain
aff001; Translational Research and Experimental Medicine, Takeda Pharmaceuticals, Cambridge, Massachusetts, United States of America
aff002
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0223109
Souhrn
Sign and goal tracker animals show different behavioral patterns in response to conditioned stimuli, which may be driven by different neural circuits involved in processing stimuli. Here, we explored whether sign and goal-tracker profiles implicated different brain regions and responses to incentive salience of stimuli. We performed three experiments using male Wistar rats. Experiment 1 showed that lesioning the medial prefrontal cortex increased the prevalence of the goal-tracker phenotype. Experiment 2 assessed the developmental trajectory of the salience incentive attribution to a conditioned stimulus, showing that increased incentive salience of stimuli increased the prevalence of the sign-tracker phenotype in mature, but not preadolescent rats. In experiment 3, the functional impact of the medial prefrontal cortex circuits was analyzed with a latent inhibition procedure. Sign tracker rats showed a reduced latent inhibition to stimuli previously exposed when compared to goal tracker or intermediate rats. The overall results of this study highlight a key role of the medial prefrontal cortex for sign tracking behavior. The expression of sign and goal tracker phenotypes changed after lesion to the medial prefrontal cortex (experiment 1), differed across development (experiment 2), and showed differences in the attentional processes to previously exposed stimuli, as preexposure to CS was ineffective in sign tracker animals (experiment 3). These data indicate that the responses to the incentive salience of stimuli in sign tracker and goal tracker profiles are likely driven by different neural circuitry, with a different role of prefrontal cortical function.
Klíčová slova:
Animal behavior – Animal performance – Behavior – Behavioral conditioning – Phenotypes – Prefrontal cortex – Rats – Magazines
Zdroje
1. Pearce JM, Hall G. A model for Pavlovian learning: variations in the effectiveness of conditioned but not of unconditioned stimuli. Psychol Rev. 1980;87: 532–52. Available: http://www.ncbi.nlm.nih.gov/pubmed/7443916 7443916
2. Pearce JM. Evaluation and development of a connectionist theory of configural learning [Internet]. Animal Learning and Behavior. Springer-Verlag; 2002. pp. 73–95. doi: 10.3758/BF03192911
3. Rescorla R, Wagner A. A theory of Pavlovian conditioning: Variations in the effectiveness of reinforcement and nonreinforcement. Classical conditioning: current research and theory, Vol 2. 1972. pp. 64–99. doi: 10.1101/gr.110528.110
4. Boakes R. Performance on learning to associate a stimulus with positive reinforcement. In: Davis H, Hurvitz H, editor. Operant Pavlovian interactions. Hillsdale, NJ: Erlbaum Associate; 1977. pp. 67–97.
5. Flagel SB, Watson SJ, Robinson TE, Akil H. Individual differences in the propensity to approach signals vs goals promote different adaptations in the dopamine system of rats. Psychopharmacology (Berl). Springer-Verlag; 2007;191: 599–607. doi: 10.1007/s00213-006-0535-8 16972103
6. Flagel SB, Robinson TE, Clark JJ, Clinton SM, Watson SJ, Seeman P, et al. An Animal Model of Genetic Vulnerability to Behavioral Disinhibition and Responsiveness to Reward-Related Cues: Implications for Addiction. Neuropsychopharmacol 2009 352. Nature Publishing Group; 2009;35: 388. doi: 10.1038/npp.2009.142 19794408
7. Flagel SB, Clark JJ, Robinson TE, Mayo L, Czuj A, Willuhn I, et al. A selective role for dopamine in stimulus–reward learning. Nature. Nature Publishing Group; 2011;469: 53–57. doi: 10.1038/nature09588 21150898
8. Flagel SB, Waselus M, Clinton SM, Watson SJ, Akil H. Antecedents and consequences of drug abuse in rats selectively bred for high and low response to novelty. Neuropharmacology. Pergamon; 2014;76: 425–436. doi: 10.1016/j.neuropharm.2013.04.033 23639434
9. Flagel SB, Robinson TE. Neurobiological basis of individual variation in stimulus-reward learning. Curr Opin Behav Sci. Elsevier; 2017;13: 178–185. doi: 10.1016/j.cobeha.2016.12.004 28670608
10. Lopez JC, Karlsson R-M, O’Donnell P. Dopamine D2 Modulation of Sign and Goal Tracking in Rats. Neuropsychopharmacol 2015 409. Nature Publishing Group; 2015;40: 2096. doi: 10.1038/npp.2015.68 25759299
11. Sarter M, Phillips KB. The Neuroscience of Cognitive-Motivational Styles: Sign- and Goal-Trackers as Animal Models. Behav Neurosci 2018, Vol 132, Pages 1–12. American Psychological Association (APA); 2018;132: 1–12. doi: 10.1037/bne0000226 29355335
12. Flagel SB, Chaudhury S, Waselus M, Kelly R, Sewani S, Clinton SM, et al. Genetic background and epigenetic modifications in the core of the nucleus accumbens predict addiction-like behavior in a rat model. Proc Natl Acad Sci U S A. National Academy of Sciences; 2016;113: E2861–70. doi: 10.1073/pnas.1520491113 27114539
13. O’Donnell P. Adolescent Onset of Cortical Disinhibition in Schizophrenia: Insights From Animal Models. Schizophr Bull. Narnia; 2011;37: 484–492. doi: 10.1093/schbul/sbr028 21505115
14. Goto Y, O’Donnell P. Delayed mesolimbic system alteration in a developmental animal model of schizophrenia. J Neurosci. 2002;22: 9070–7. Available: http://www.ncbi.nlm.nih.gov/pubmed/12388614 12388614
15. Berridge KC. The debate over dopamine’s role in reward: the case for incentive salience. Psychopharmacology (Berl). 2007;191: 391–431. doi: 10.1007/s00213-006-0578-x 17072591
16. Berridge KC, Robinson TE. What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Rev. Elsevier; 1998;28: 309–369. doi: 10.1016/S0165-0173(98)00019-8
17. Goto Y, Grace AA. Limbic and cortical information processing in the nucleus accumbens. Trends Neurosci. Elsevier Current Trends; 2008;31: 552–558. doi: 10.1016/j.tins.2008.08.002 18786735
18. O’Donnell P, Grace AA. Synaptic interactions among excitatory afferents to nucleus accumbens neurons: hippocampal gating of prefrontal cortical input. J Neurosci. Society for Neuroscience; 1995;15: 3622–39. doi: 10.1523/JNEUROSCI.15-05-03622.1995 7751934
19. Gray J., Moran P., Grigoryan G, Peters S., Young AM., Joseph M. Latent inhibition: the nucleus accumbens connection revisited. Behav Brain Res. Elsevier; 1997;88: 27–34. doi: 10.1016/s0166-4328(97)02313-9 9401705
20. Groenewegen H, Mulder AB, Beijer AVJ, Wright CI, Wpes FH, Silva DA, et al. Hippocampal and amygdaloid interactions in the nucleus accumbens [Internet]. Psychobiology. Springer-Verlag; 1999. doi: 10.3758/bf03332111
21. Haber SN, Fudge JL, McFarland NR. Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. J Neurosci. Society for Neuroscience; 2000;20: 2369–82. doi: 10.1523/JNEUROSCI.20-06-02369.2000 10704511
22. Kunishio K, Haber SN. Primate cingulostriatal projection: Limbic striatal versus sensorimotor striatal input. J Comp Neurol. John Wiley & Sons, Ltd; 1994;350: 337–356. doi: 10.1002/cne.903500302 7533796
23. Lavín A, Grace AA. Modulation of dorsal thalamic cell activity by the ventral pallidum: Its role in the regulation of thalamocortical activity by the basal ganglia. Synapse. John Wiley & Sons, Ltd; 1994;18: 104–127. doi: 10.1002/syn.890180205 7839311
24. Saunders BT, Robinson TE. The role of dopamine in the accumbens core in the expression of Pavlovian-conditioned responses. Eur J Neurosci. NIH Public Access; 2012;36: 2521–32. doi: 10.1111/j.1460-9568.2012.08217.x 22780554
25. Pérez-Díaz F, Díaz E, Sánchez N, Vargas JP, Pearce JM, López JC. Different involvement of medial prefrontal cortex and dorso-lateral striatum in automatic and controlled processing of a future conditioned stimulus. PLoS One. Public Library of Science; 2017;12: e0189630. doi: 10.1371/journal.pone.0189630 29240804
26. Homayoun H, Moghaddam B. Differential representation of Pavlovian-instrumental transfer by prefrontal cortex subregions and striatum. Eur J Neurosci. NIH Public Access; 2009;29: 1461–76. doi: 10.1111/j.1460-9568.2009.06679.x 19309320
27. Hearst Eliot, Jenkins HM. Sign-tracking: the stimulus-reinforcer relation and directed action [Internet]. Austin Tex.: Psychonomic Society; 1974. Available: https://www.worldcat.org/title/sign-tracking-the-stimulus-reinforcer-relation-and-directed-action/oclc/1895085
28. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. Elsevier; 2007.
29. Schoenbaum G, Setlow B, Saddoris MP, Gallagher M. Encoding predicted outcome and acquired value in orbitofrontal cortex during cue sampling depends upon input from basolateral amygdala. Neuron. Elsevier; 2003;39: 855–67. doi: 10.1016/s0896-6273(03)00474-4 12948451
30. Meyer PJ, Lovic V, Saunders BT, Yager LM, Flagel SB, Morrow JD, et al. Quantifying Individual Variation in the Propensity to Attribute Incentive Salience to Reward Cues. PLoS One. Public Library of Science; 2012;7: e38987. doi: 10.1371/journal.pone.0038987 22761718
31. Caballero A, Tseng KY. GABAergic Function as a Limiting Factor for Prefrontal Maturation during Adolescence. Trends Neurosci. Elsevier Current Trends; 2016;39: 441–448. doi: 10.1016/j.tins.2016.04.010 27233681
32. Caballero A, Flores-Barrera E, Cass DK, Tseng KY. Differential regulation of parvalbumin and calretinin interneurons in the prefrontal cortex during adolescence. Brain Struct Funct. NIH Public Access; 2014;219: 395–406. doi: 10.1007/s00429-013-0508-8 23400698
33. Berridge KC. Reward learning: Reinforcement, incentives, and expectations. Psychol Learn Motiv. Academic Press; 2000;40: 223–278. doi: 10.1016/S0079-7421(00)80022-5
34. Toates FM ( Frederick M. Motivational systems [Internet]. Cambridge: Cambridge University Press; 1986. Available: https://www.worldcat.org/title/motivational-systems/oclc/924949860
35. Franken IHA, Booij J, van den Brink W. The role of dopamine in human addiction: From reward to motivated attention. Eur J Pharmacol. Elsevier; 2005;526: 199–206. doi: 10.1016/j.ejphar.2005.09.025 16256105
36. Robinson TE, Berridge KC. The neural basis of drug craving: An incentive-sensitization theory of addiction. Brain Res Rev. Elsevier; 1993;18: 247–291. doi: 10.1016/0165-0173(93)90013-P 8401595
37. Haight JL, Fuller ZL, Fraser KM, Flagel SB. A food-predictive cue attributed with incentive salience engages subcortical afferents and efferents of the paraventricular nucleus of the thalamus. Neuroscience. Pergamon; 2017;340: 135–152. doi: 10.1016/j.neuroscience.2016.10.043 27793779
38. Haight JL, Flagel SB. A potential role for the paraventricular nucleus of the thalamus in mediating individual variation in Pavlovian conditioned responses. Front Behav Neurosci. Frontiers Media SA; 2014;8: 79. doi: 10.3389/fnbeh.2014.00079 24672443
39. Belin D, Balado E, Piazza PV, Deroche-Gamonet V. Pattern of Intake and Drug Craving Predict the Development of Cocaine Addiction-like Behavior in Rats. Biol Psychiatry. Elsevier; 2009;65: 863–868. doi: 10.1016/j.biopsych.2008.05.031 18639867
40. Haber SN. Corticostriatal circuitry. Dialogues Clin Neurosci. Les Laboratoires Servier; 2016;18: 7–21. Available: http://www.ncbi.nlm.nih.gov/pubmed/27069376 27069376
41. Campus P, Accoto A, Maiolati M, Latagliata C, Orsini C. Role of prefrontal 5-HT in the strain-dependent variation in sign-tracking behavior of C57BL/6 and DBA/2 mice. Psychopharmacology (Berl). Springer Berlin Heidelberg; 2016;233: 1157–1169. doi: 10.1007/s00213-015-4192-7 26728892
42. Tomie A, Grimes KL, Pohorecky LA. Behavioral characteristics and neurobiological substrates shared by Pavlovian sign-tracking and drug abuse. Brain Res Rev. NIH Public Access; 2008;58: 121–35. doi: 10.1016/j.brainresrev.2007.12.003 18234349
43. Pitchers KK, Sarter M, Robinson TE. The hot “n” cold of cue-induced drug relapse. Learn Mem. Cold Spring Harbor Laboratory Press; 2018;25: 474–480. doi: 10.1101/lm.046995.117 30115769
44. Vargas JP, Díaz E, Portavella M, López JC. Animal Models of Maladaptive Traits: Disorders in Sensorimotor Gating and Attentional Quantifiable Responses as Possible Endophenotypes. Front Psychol. Frontiers; 2016;7: 206. doi: 10.3389/fpsyg.2016.00206 26925020
Článek vyšel v časopise
PLOS One
2019 Číslo 9
- Proč se v Česku šíří několik „vymýcených“ infekcí najednou? Ptáme se odborníků
- ADHD jako evoluční výhoda? Výzkum se zaměřil na lovce a sběrače
- Není migréna jako migréna: Co pociťují ženy a co muži?
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Není statin jako statin aneb praktický přehled rozdílů jednotlivých molekul
Nejčtenější v tomto čísle
- Graviola (Annona muricata) attenuates behavioural alterations and testicular oxidative stress induced by streptozotocin in diabetic rats
- CH(II), a cerebroprotein hydrolysate, exhibits potential neuro-protective effect on Alzheimer’s disease
- Comparison between Aptima Assays (Hologic) and the Allplex STI Essential Assay (Seegene) for the diagnosis of Sexually transmitted infections
- Assessment of glucose-6-phosphate dehydrogenase activity using CareStart G6PD rapid diagnostic test and associated genetic variants in Plasmodium vivax malaria endemic setting in Mauritania
Zvyšte si kvalifikaci online z pohodlí domova
Všechny kurzy