Publikationsserver der Universitätsbibliothek Marburg

Titel:Incentive motivation and ultrasonic vocalizations in rats
Autor:Brenes Sáenz, Juan Carlos
Weitere Beteiligte: Schwarting, Rainer (Prof. Dr.)
Veröffentlicht:2015
URI:https://archiv.ub.uni-marburg.de/diss/z2015/0234
URN: urn:nbn:de:hebis:04-z2015-02340
DOI: https://doi.org/10.17192/z2015.0234
DDC:150 Psychologie
Titel (trans.):Ultraschallvokalisation und Anreizmotivation bei Ratten
Publikationsdatum:2015-05-28
Lizenz:https://rightsstatements.org/vocab/InC-NC/1.0/

Dokument

Schlagwörter:
Ultrasonic Vocalization, Vokalisation, Ultraschall, Motivation, Motivation

Summary:
After experiencing a reward, the positive affective reactions it induces can become associated with its sensory properties and related cues. However, the manner in which such affective reward representations are expressed in animals remains unclear. Juvenile and adult rats communicate through ultrasonic vocalizations (USVs), which also serve as situation-dependent affective signals. Since rats emit high frequency (i.e., 50-kHz) USVs in socially and non-socially rewarding situations, 50-kHz calls might prove to be a way incentive motivational state is signaled when training rats to anticipate food rewards under some predictable cues. In general, the results show that reward-cues become effective to elicit 50-kHz calls. Under certain conditions, however, the utterance of 50-kHz calls can be either suppressed during a highly motivational state, or more strikingly, can be elicited when food rewards were devalued by satiation. For rats, both a state of hunger and waiting for access to a daily meal can be negatively perceived if the food reward offered turns out to be less satisfying than expected. Learning to anticipate such a negative state seemed to suppress the otherwise positive affective reactions evoked by having access to a highly expected food. Such a frustration-like effect occurred only at the USVs level without being indicated behaviourally through changes in rats’ learning and motivation to approach and consume the reward. In contrast, providing continued access to the reward prevented the suppression of USVs. Surprisingly, in spite of being sated and no longer interested in seeking and consuming the reward, rats nevertheless continued to emit appetitive USVs in the presence of cues predicting a previously desired food. Rats as a whole, just as with humans, seem to represent rewards affectively beyond basal appetite requirements. However, the ability to attribute incentive salience to reward cues has been shown to strongly differ among individuals. The second study, therefore, focused on the analysis of individual differences in conditioned anticipatory activity elicited by reward-related cues as indicative of the predisposition of animals to attribute incentive salience to otherwise neutral stimuli. Across several experiments, individual rats prone to attribute incentive salience to reward cues –as indicated by high levels of either rearing activity, or sign-tracking behavior– showed heightened reward-induced affective responses, namely in the form of 50-kHz calls. When re-exposing rats to reward cues after a non-testing period, USVs were elicited even at higher rates than previously, especially in subjects prone to attributing incentive salience to reward cues. USVs appeared reliably expressed over time and persisted despite physiological needs have already been fulfilled. Interestingly, USVs were still elicited by reward cues even though reward-oriented behaviors and exploratory activity were drastically weakened by reward devaluation. Additionally, prone subjects seemed to undergo particular adaptations in their dopaminergic system related to incentive learning, as indicated by the attenuated response to the catecholamine agonist amphetamine and to the dopamine receptor antagonist flupenthixol. The investigation of the psychological and neurobiological factors underlying affective states as related to incentive motivation is of remarkable relevance in preclinical- and clinical-oriented research. The current findings may have translational potential, since for some individuals, excessive attribution of incentive salience to reward cues may lead to compulsive behavior disorders, such as overeating, pathological gambling, and drug addiction. Certain aspects of these disabling human conditions can be further investigated with the same animal models as implemented in the present studies.

Bibliographie / References

  1. Holland PC. Origins of behavior in Pavlovian conditioning. In: Medin DL, editor. The Psychology of Learning and Motivation (vol. 18), San Diego: Academic; 1984, p. 129–74.
  2. Fiorillo CD, Tobler PN, Schultz W. Discrete coding of reward probability and uncertainty by dopamine neurons. Science 2003;299:1898–902.
  3. Pawlak CR, Schwarting RKW. Repeated nicotine treatment in rats with high versus low rearing activity: analyses of behavioural sensitisation and place preference. Psychopharmacology 2005;178:440–50.
  4. Smith MA, Walker KL, Cole KT, Lang KC. The effects of aerobic exercise on cocaine self- administration in male and female rats. Psychopharmacology 2011;218:357–69.
  5. Wöhr M, Schwarting RKW. Affective communication in rodents: ultrasonic vocalizations as a tool for research on emotion and motivation. Cell Tissue Res 2013;254:81–97.
  6. Burgdorf J, Panksepp J, Brudzynski SM, Kroes R, Moskal JR. Breeding for 50-kHz positive affective vocalization in rats. Behav Genetics 2005;35:67–72.
  7. Schwarting RKW, Jegan N, Wöhr M. Situational factors, conditions and individual variables which can determine ultrasonic vocalizations in male adult Wistar rats. Behav Brain Res 2007;182:208–22.
  8. Natusch C, Schwarting RKW. Using bedding in a test environment critically affects 50-kHz ultrasonic vocalizations in laboratory rats. Pharmacol Biochem Behav 2010;96:251–59.
  9. Balleine BW. Neural bases of food-seeking: Affect, arousal and reward in corticostriatolimbic circuits. Physiol Behav 2005;86:717–30.
  10. Knutson B, Burgdorf J, Panksepp J. High-frequency ultrasonic vocalization index conditioned pharmacological reward. Physiol Behav 1999;66:639–43.
  11. Tomie A, Aguado AS, Pohorecky LA, Benjamin D. Individual differences in pavlovian autoshaping of lever pressing in rats predict stress-induced corticosterone release and mesolimbic levels of monoamines. Pharmacol Biochem Behav 2000;65:509–17.
  12. Laviolette SR, Nader K, van der Kooy D. Motivational state determines the functional role of the mesolimbic dopamine system in the mediation of opiate reward processes. Behav Brain Res 2002;129:17–29.
  13. Burgdorf J, Knutson B, Panksepp J, Ikemoto S. Nucleus accumbens amphetamine microinjections unconditionally elicit 50 kHz ultrasonic vocalizations in rats. Behav Neurosci 2001;115:940–44.
  14. Burgdorf J, Kroes RA, Moskal JR, Pfaus JG, Brudzynski SM, Panksepp J. Ultrasonic vocalizations of rats (Rattus norvegicus) during mating, play, and aggression: Behavioral concomitants, relationship to reward, and self-administration of playback. J Comp Psychol 2008;122:357–67.
  15. Thomas DA, Howard SB, Barfield RJ. Male produced ultrasonic vocalizations and mating patterns in female rats. J Comp Psychol 1982;96:807–15.
  16. Johnson PM, Kenny PJ. Dopamine D2 receptors in addiction-like reward dysfunction and compulsive eating in obese rats. Nat Neurosci 2010;13:635–41.
  17. Brenes JC, Schwarting RKW. Attribution and expression of incentive salience are differentially signaled by ultrasonic vocalizations in rats. PloS ONE 2014. 9(7): e102414.
  18. Solinas M, Thiriet N, Chauvet C, Jaber M. Prevention and treatment of drug addiction by environmental enrichment. Prog Neurobiol 2010;92:572–92.
  19. Bindra D. How adaptive behavior is produced: a perceptual-motivation alternative to response reinforcement. Behav Brain Sci 1978;1:41–91.
  20. Cain ME, Mersmann MG, Gill MJ, Pittenger ST. Dose-dependent effects of differential rearing on amphetamine-induced hyperactivity. Behav Pharmacol 2012;23:744–53.
  21. Woolverton WL, Kandel D, Schuster CR. Tolerance and cross-tolerance to cocaine and d- amphetamine. J Pharmacol Exp Ther 1978;205:525–35.
  22. Williams SN, Undieh AS. Brain-derived neurotrophic factor signaling modulates cocaine induction of reward-associated ultrasonic vocalization in rats. J Pharmacol Exp Ther 2010;332:463–68.
  23. 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 2007;191:599–607.
  24. Wright JM, Gourdon JC, Clarke PBS. Identification of multiple call categories within the rich repertoire of adult rat 50-kHz ultrasonic vocalizations: effects of amphetamine and social context. Psychopharmacology 2010;211:1–13.
  25. Wright JM, Dobosiewicz MR, Clarke PB. The role of dopaminergic transmission through D1-like and D2-like receptors in amphetamine-induced rat ultrasonic vocalizations. Psychopharmacology 2013;225:853–68.
  26. Pereira M, Andreatini R, Schwarting RKW, Brenes JC. Amphetamine-induced appetitive 50-kHz calls in rats: a genuine affective marker of mania? Psychopharmacology DOI 10.1007/s00213-013-3413-1.
  27. Roseboom PH, Gnegy ME. Acute in vivo amphetamine produces a homologous desensitization of dopamine receptor coupled adenylate cyclase activities and decreases agonist binding to the Dl site. Mol Pharmacol 1988;34:148–56.
  28. Appendix C: Curriculum Vitae 161
  29. Rescorla RA, Wagner AR. A theory of Pavlovian conditioning: variations in the effectiveness of reinforcement and nonreinforcement. In: Black AH, Prokasy WF, editors. Classical Conditioning II, New York: Appleton-Century-Crofts; 1972, p. 64–99.
  30. Barker DJ, Root DH, Ma S, Jha S, Megehee L, Pawlak AP, et al. Dose-dependent differences in short ultrasonic vocalizations emitted by rats during cocaine self- administration. Psychopharmacology 2010;211:435–42.
  31. Experimental design Brenes, J.C. Execution of the experiments Brenes, J.C.
  32. Schachter S. Obesity and eating. Internal and external cues differentially affect eating behavior of obese and normal subjects. Science 1968;161:751–56.
  33. Simola N, Fenu S, Costa G, Pinna A, Plumitallo A, Morelli M. Pharmacological characterization of 50-kHz ultrasonic vocalizations in rats: comparison of the effects of different psychoactive drugs and relevance in drug-induced reward. Neuropharmacology 2012;63:224–34.
  34. Data analysis Brenes, J.C. Preparation of the manuscript Brenes, J.C.
  35. Dickinson A, Balleine BW. The role of learning in the operation of motivational systems. In: Gallistel CR, editor. Learning, motivation and emotion, volume 3 of Steven's handbook of experimental psychology (3rd ed), New York: John Wiley & Sons; 2002, p. 497–533.
  36. Mällo T, Matrov D, Herm L, Kõiv K, Eller M, Rinken A, et al. Tickling-induced 50-kHz ultrasonic vocalization is individually stable and predicts behaviour in tests of anxiety and depression in rats. Behav Brain Res 2007;184:57–71.
  37. Burgdorf J, Panksepp J, Brudzynski SM, Beinfeld MC, Cromwell HC, Kroes RA, et al. The effects of selective breeding for differential rates of 50-kHz ultrasonic vocalizations on emotional behaviour in rats. Dev Psychobiol 2009;51:34–46.
  38. Burgdorf J, Knutson B, Panksepp J. Anticipation of rewarding electrical brain stimulation evokes ultrasonic vocalization in rats. Behav Neurosci 2000;114:320–27.
  39. Davis JF, Tracy AL, Schurdak JD, Tschop MH, Lipton JW, Clegg DJ, et al. Exposure to elevated levels of dietary fat attenuates psychostimulant reward and mesolimbic dopamine turnover in the rat. Behav Neurosci 2008;122:1257–63.
  40. Brudzynski SM, Pniak A. Social contacts and production of 50-kHz short ultrasonic calls in adult tats. J Comp Psychol 2002;116:73–82.
  41. Ikemoto S, Panksepp J. Dissociations between appetitive and consummatory responses by pharmacological manipulations of reward-relevant brain regions. Behav Neurosci 1996;110:331–45.
  42. Barbano MF, Cador M. Various aspects of feeding behavior can be partially dissociated in the rat by the incentive properties of food and the physiological state. Behav Neurosci 2005;119:1244–53.
  43. Rescorla RA. Behavioral studies of Pavlovian conditioning. Ann Rev Neurosci 1988;11:329–52.
  44. Flagel SB, Clark JJ, Robinson TE, Mayo L, Czuj A, Willuhn I, et al. A selective role for dopamine in stimulus-reward learning. Nature 2011;469:53–7.
  45. Barbano MF, Cador M. Differential regulation of the consummatory, motivational and anticipatory aspects of feeding behavior by dopaminergic and opioidergic drugs. Neuropsychopharmacology 2006;31:1371–81.
  46. Ahrens AM, Nobile CW, Page LE, Maier EY, Duvauchelle CL, Schallert T. Individual differences in the conditioned and unconditioned rat 50-kHz ultrasonic vocalizations elicited by repeated amphetamine exposure. Psychopharmacology 2013;229:687–700.
  47. Jenkins HM, Moore BR. The form of the auto-shaped response with food or water reinforcers. J Exp Anal Behav 1973;20:163–81.
  48. Smith MA, Schmidt KT, Iordanou JC, Mustroph ML. Aerobic exercise decreases the positive-reinforcing effects of cocaine. Drug Alcohol Depend 2008;98:129–35.
  49. Robinson, TE, Flagel SB. Dissociating the predictive and incentive motivational properties of reward-related cues through the study of individual differences. Biol Psychiatry 2009;65:869–73.
  50. Ma ST, Maier EY, Ahrens AM, Schallert T, Duvauchelle CL. Repeated intravenous cocaine experience: development and escalation of pre-drug anticipatory 50-kHz ultrasonic vocalizations in rats. Behav Brain Res 2010;212:109–14.
  51. Berridge KC. From prediction error to incentive salience: mesolimbic computation of reward motivation. Eur J Neurosci 2012;35:1124–43.
  52. Rygula R, Pluta H, Popik P. Laughing Rats Are Optimistic. PLoS ONE 2012;7(12): e51959.
  53. Meyer PJ, Ma ST, Robinson TE. A cocaine cue is more preferred and evokes more frequency-modulated 50-kHz ultrasonic vocalizations in rats prone to attribute incentive salience to a food cue. Psychopharmacology 2012;219:999–1009.
  54. Dalley JW, Laane K, Theobald DE, Armstrong HC, Corlett PR, Chudasama Y, et al. Time- limited modulation of appetitive Pavlovian memory by D1 and NMDA receptors in the nucleus accumbens. Proc Natl Acad Sci USA 2005;102:6189–94.
  55. Cornell CE, Rodin J, Weingarten H. Stimulus-induced eating when satiated. Physiol Behav 1989;45:695–704.
  56. Volkow ND, Wang GJ, Tomasi D, Baler RD. The addictive dimensionality of obesity. Biol Psychiatry 2013;73:811–18.
  57. Browning JR, Browning DA, Maxwell AO, Dong Y, Jansen HT, Panksepp J, et al. Positive affective vocalizations during cocaine and sucrose self-administration: a model for spontaneous drug desire in rats. Neuropharmacology 2011;61:268–75.
  58. Robinson TE, Yager LM, Cogan ES, Saunders BT. On the motivational properties of reward cues: Individual differences. Neuropharmacology 2014;76:450–59.
  59. Burgdorf J, Panksepp J. Tickling induces reward in adolescent rats. Physiol Behav 2001;72:167–73.
  60. Petrovich GD, Ross CA, Gallagher M, Holland PC. Learned contextual cue potentiates eating in rats. Physiol Behav 2007;90:362–67.
  61. Wöhr M, Houx B, Schwarting RKW, Spruijt B. Effects of experience and context on 50-kHz vocalizations in rats. Physiol Behav 2008;93:766–76.
  62. Berridge KC. Reward learning: reinforcement, incentives, and expectations. In: Medin DL, editor. Psychology of learning and motivation (vol. 40), New York: Academic Press; 2001, p. 223–78.
  63. Wintink AJ, Brudzynski SM. The related roles of dopamine and glutamate in the initiation of 50-kHz ultrasonic calls in adult rats. Pharmacol Biochem Behav 2001;70:317–23.
  64. Lett BT, Grant VL, Koh MT, Flynn G. Prior experience with wheel running produces cross- tolerance to the rewarding effect of morphine. Pharmacol Biochem Behav 2002;72:101–05.
  65. Cosgrove KP, Hunter RG, Carroll ME. Wheel-running attenuates intravenous cocaine self- administration in rats: sex differences. Pharmacol Biochem Behav 2002;73:663–71.
  66. Pawlak CR, Ho YJ, Schwarting RKW. Animal models of human psychopathology based on individual differences in novelty-seeking and anxiety. Neurosci Biobehav Rev 2008;32:1544–68.
  67. Burgdorf J, Wood PL, Kroes R, Moskal JR, Panksepp J. Neurobiology of 50-kHz ultrasonic vocalizations in rats: Electrode mapping, lesion, and pharmacological studies. Behav Brain Res 2007;182:274–83.
  68. Ahrens AM, Ma ST, Maier EY, Duvauchelle CL, Schallert T. Repeated intravenous amphetamine exposure: rapid and persistent sensitization of 50-kHz ultrasonic trill calls in rats. Behav Brain Res 2009;197:205–9.
  69. Yager LM, Robinson TE. Cue-induced reinstatement of food seeking in rats that differ in their propensity to attribute incentive salience to food cues. Behav Brain Res 2010;214:30– 4.
  70. Maier EY, Ahrens AM, Ma ST, Schallert T, Duvauchelle CL. Cocaine deprivation effect: cue abstinence over weekends boosts anticipatory 50-kHz ultrasonic vocalizations in rats. Behav Brain Res 2010;214:75–9.
  71. Brudzynski SM, Silkstone M, Komadoski M, Scullion K, Duffus S, Burgdorf J, et al. Effects of intraaccumbens amphetamine on production of 50 kHz vocalizations in three lines of selectively bred Long-Evans rats. Behav Brain Res 2011;217:32–40.
  72. Anselme P, Robinson MJF, Berridge KC. Reward uncertainty enhances incentive salience attribution as sign-tracking. Behav Brain Res 2013;238:53–61.
  73. Nair SG, Adams-Deutsch T, Epstein DH, Shaham Y. The neuropharmacology of relapse to food seeking: methodology, main findings, and comparison with relapse to drug seeking. Prog Neurobiol 2009;89:18–45.
  74. Mu P, Fuchs T, Saal DB, Sorg BA, Dong Y, Panksepp J. Repeated cocaine exposure induces sensitization of ultrasonic vocalization in rats. Neurosci Lett 2009;453:31–5.
  75. Thiel CM, Müller CP, Huston JP, Schwarting RKW. High versus low reactivity to a novel environment: behavioural, pharmacological and neurochemical assessments. Neuroscience 1999;93:243–51.
  76. Noble EP. Addiction and its reward process through polymorphisms of the D2 dopamine receptor gene: A review. Eur Psychiatry 2000;15:79–89.
  77. Robinson MJF, Berridge KC. Instant transformation of learned repulsion into motivational ''wanting''. Curr Biol 2013;23:282–89.
  78. Smith MA, Pitts EG. Wheel running decreases the positive reinforcing effects of heroin. Pharmacol Rep 2012;64:960–64.
  79. Blundell JE, Latham CJ, Moniz E, McArthur RA, Rogers PJ. Structural analysis of the actions of amphetamine and fenfluramine on food intake and feeding behaviour in animals and in man. Curr Med Res Opin 1979;6:34–54.


* Das Dokument ist im Internet frei zugänglich - Hinweise zu den Nutzungsrechten