Learning and Motivational Processes Contributing to Pavlovian–Instrumental Transfer and Their Neural Bases: Dopamine and Beyond

  • Laura H. Corbit
  • Bernard W. BalleineEmail author
Part of the Current Topics in Behavioral Neurosciences book series (CTBN, volume 27)


Pavlovian stimuli exert a range of effects on behavior from simple conditioned reflexes, such as salivation, to altering the vigor and direction of instrumental actions. It is currently accepted that these distinct behavioral effects stem from two sources (i) the various associative connections between predictive stimuli and the component features of the events that these stimuli predict and (ii) the distinct motivational and cognitive functions served by cues, particularly their arousing and informational effects on the selection and performance of specific actions. Here, we describe studies that have assessed these latter phenomena using a paradigm that has come to be called Pavlovian–instrumental transfer. We focus first on behavioral experiments that have described distinct sources of stimulus control derived from the general affective and outcome-specific predictions of conditioned stimuli, referred to as general transfer and specific transfer, respectively. Subsequently, we describe research efforts attempting to establish the neural bases of these transfer effects, largely in the afferent and efferent connections of the nucleus accumbens (NAc) core and shell. Finally, we examine the role of predictive cues in examples of aberrant stimulus control associated with psychiatric disorders and addiction.


Instrumental learning Pavlovian learning Nucleus accumbens Amygdala Reward Incentive 



This preparation of this chapter was supported by a Project Grant (APP1050137) to LHC and by a Senior Principal Research Fellowship to BWB, each from the National Health and Medical Research Council of Australia.


  1. Apicella P (2007) Leading tonically active neurons of the striatum from reward detection to context recognition. Trends Neurosci 30:299–306CrossRefPubMedGoogle Scholar
  2. Balleine BW (1994) Asymmetrical interactions between thirst and hunger in Pavlovian-instrumental transfer. Q J Exp Psychol B 47:211–231PubMedGoogle Scholar
  3. Balleine BW, Morris RW, Leung BK (2015) Thalamocortical integration of instrumental learning and performance and their disintegration in addiction. Brain Res (Epub ahead of print)Google Scholar
  4. Baxter DJ, Zamble E (1982) Reinforcer and response specificity in appetitive transfer of control. Anim Learn Behav 10:201–210CrossRefGoogle Scholar
  5. Beck A, Wustenberg T, Genauck A, Wrase J, Schlagenhauf F, Smolka et al (2012) Effect of brain structure, brain function, and brain connectivity on relapse in alcohol-dependent patients. Arch Gen Psychiatry 69:842–852CrossRefPubMedGoogle Scholar
  6. Berridge KC (2007) The debate over dopamine’s role in reward: the case for incentive salience. Psychopharmacology 191:391–431CrossRefPubMedGoogle Scholar
  7. Bertran-Gonzalez J, Laurent V, Chieng BC, Christie MJ, Balleine BW (2013) Learning-related translocation of δ-opioid receptors on ventral striatal cholinergic interneurons mediates choice between goal-directed actions. J Neurosci 33:16060–16071CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bindra D (1974) A motivational view of learning, performance, and behaviour modification. Psychol Rev 81:199–213CrossRefPubMedGoogle Scholar
  9. Bindra D (1978) How adaptive behavior is produced: a perceptual motivational alternative to response-reinforcement. Behav Brain Sci 1:41–91CrossRefGoogle Scholar
  10. Blundell P, Hall G, Killcross S (2001) Lesions of the basolateral amygdala disrupt selective aspects of reinforcer representation in rats. J Neurosci 21(22):9018–9026Google Scholar
  11. Brown P (2007) Abnormal oscillatory synchronisation in the motor system leads to impaired movement. Curr Opin Neurobiol 17:656–664CrossRefPubMedGoogle Scholar
  12. Brown MT, Tan KR, O’Connor EC, Nikonenko I, Muller D, Lüscher C (2012) Ventral tegmental area GABA projections pause accumbal cholinergic interneurons to enhance associative learning. Nature 492:452–456CrossRefPubMedGoogle Scholar
  13. Campese V, McCue M, Lázaro-Muñoz G, Ledoux JE, Cain CK (2013) Development of an aversive Pavlovian-to-instrumental transfer task in rat. Front Behav Neurosci 7:176CrossRefPubMedPubMedCentralGoogle Scholar
  14. Colwill RM, Rescorla RA (1990) Effect of reinforcer devaluation on discriminative control of instrumental behavior. J Exp Psychol Anim Behav Process 16(1):40Google Scholar
  15. Colwill RM, Motzkin DK (1994) Encoding of the unconditioned stimulus in Pavlovian conditioning. Anim Learn Behav 22:384–394CrossRefGoogle Scholar
  16. Corbit LH, Balleine BW (2005) Double dissociation of basolateral and central amygdala lesions on the general and outcome-specific forms of Pavlovian-instrumental transfer. J Neurosci 25:962–970CrossRefPubMedGoogle Scholar
  17. Corbit LH, Balleine BW (2011) The general and outcome-specific forms of Pavlovian-instrumental transfer are differentially mediated by the nucleus accumbens core and shell. J Neurosci 31:11786–11794CrossRefPubMedPubMedCentralGoogle Scholar
  18. Corbit LH, Chieng BC, Balleine BW (2014) Effects of repeated cocaine exposure on habit learning and reversal by N-acetylcysteine. Neuropsychopharmacology 39:1893–1901CrossRefPubMedPubMedCentralGoogle Scholar
  19. Corbit LH, Janak PH (2007a) Inactivation of the lateral but not medial dorsal striatum eliminates the excitatory impact of Pavlovian stimuli on instrumental responding. J Neurosci 27:13977–13981CrossRefPubMedGoogle Scholar
  20. Corbit LH, Janak PH (2007b) Ethanol-associated cues produce general Pavlovian-instrumental transfer. Alcohol Clin Exp Res 31:766–774CrossRefPubMedGoogle Scholar
  21. Corbit LH, Janak PH (2010) Posterior dorsomedial striatum is critical for both selective instrumental and Pavlovian reward learning. Eur J Neurosci 31:1312–1321CrossRefPubMedPubMedCentralGoogle Scholar
  22. Corbit LH, Janak PH, Balleine BW (2007) General and outcome-specific forms of Pavlovian-instrumental transfer: the effect of shifts in motivational state and inactivation of the ventral tegmental area. Eur J Neurosci 26:3141–3149CrossRefPubMedGoogle Scholar
  23. Corbit LH, Muir JL, Balleine BW (2001) The role of the nucleus accumbens in instrumental conditioning: evidence for a functional dissociation between core and shell. J Neurosci 21:3251–3260PubMedGoogle Scholar
  24. Corbit LH, Muir JL, Balleine BW (2003) Lesions of mediodorsal thalamus and anterior thalamic nuclei produce dissociable effects on instrumental conditioning in rats. Eur J Neurosci 18:1286–1294CrossRefPubMedGoogle Scholar
  25. Corbit LH, Nie H, Janak PH (2012) Habitual alcohol seeking: time course and the contribution of subregions of the dorsal striatum. Biol Psychiatry 72:389–395CrossRefPubMedPubMedCentralGoogle Scholar
  26. Cui G, Jun SB, Jin X, Pham MD, Vogel SS, Lovinger DM, Costa RM (2013) Concurrent activation of striatal direct and indirect pathways during action initiation. Nature 494:238–242CrossRefPubMedPubMedCentralGoogle Scholar
  27. de Borchgrave R, Rawlins JN, Dickinson A, Balleine BW (2002) Effects of cytotoxic nucleus accumbens lesions on instrumental conditioning in rats. Exp Brain Res 144:50–68Google Scholar
  28. Dias-Ferreira E, Sousa JC, Melo I, Morgado P, Mesquita AR, Cerqueira JJ, Costa RM, Sousa N (2009) Chronic stress causes frontostriatal reorganization and affects decision-making. Science 325:621–625CrossRefPubMedGoogle Scholar
  29. Dickinson A (1980) Contemporary animal learning theory. Cambridge University Press, CambridgeGoogle Scholar
  30. Dickinson A (1985) Actions and habits—the development of behavioral autonomy. Philos Trans R Soc Lond Ser B Biol Sci 308:67–78CrossRefGoogle Scholar
  31. Dickinson A, Balleine BW (1994) Motivational control of goal-directed action. Anim learn Behav 22:1–18CrossRefGoogle Scholar
  32. Dickinson A, Balleine BW (2002) Steven’s handbook of experimental psychology: learning, motivation and emotion. In: Gallistel C (ed) The role of learning in the operation of motivational systems, vol 3. Wiley, New York, pp 497–534Google Scholar
  33. Dickinson A, Dawson GR (1987) Pavlovian processes in the motivational control of instrumental performance. Q J Exp Psychol Sect B Comp Physiol Psychol 39:201–213Google Scholar
  34. Dickinson A, Dearing MF (1979) Appetitive-aversive interactions and inhibitory processes. In: Dickinson A, Boakes RA (eds) Mechanism of learning and motivation. Lawrence Erlbaum Associates, Hillsdale, NJ, pp 203–231Google Scholar
  35. Dickinson A, Smith J, Mirenowicz J (2000) Dissociation of Pavlovian and instrumental incentive learning under dopamine antagonists. Behav Neurosci 114:468–83Google Scholar
  36. Ding JB, Guzman JN, Peterson JD, Goldberg JA, Surmeier DJ (2010) Thalamic gating of corticostriatal signaling by cholinergic interneurons. Neuron 67:294–307CrossRefPubMedPubMedCentralGoogle Scholar
  37. Estes WK (1943) Discriminative conditioning I: a discriminative property of conditioned anticipation. J Exp Psychol 32:150–155CrossRefGoogle Scholar
  38. Fuchs RA, Branham RK, See RE (2006) Different neural substrates mediate cocaine seeking after abstinence versus extinction training: a critical role for the dorsolateral caudate-putamen. J Neurosci 26:3584–3588CrossRefPubMedPubMedCentralGoogle Scholar
  39. Furlong TM, Jayaweera HK, Balleine BW, Corbit LH (2014) Binge-like consumption of a palatable food accelerates habitual control of behavior and is dependent on activation of the dorsolateral striatum. J Neurosci 34:5012–5022CrossRefPubMedGoogle Scholar
  40. Ganesan R, Pearce JM (1988) Effect of changing the unconditioned stimulus on appetitive blocking. J Exp Psychol Anim Behav Proc 14(3):280–291Google Scholar
  41. Garbusow M, Schad DJ, Sebold M, Friedel E, Bernhardt N, Koch SP et al (2015) Pavlovian-to-instrumental transfer effects in the nucleus accumbens relate to relapse in alcohol dependence. Addict Biol (Epub ahead of print)Google Scholar
  42. Garbusow M, Schad DJ, Sommer C, Jünger E, Sebold M, Friedel E, Wendt J, Kathmann N, Schlagenhauf F, Zimmermann US, Heinz A, Huys QJ, Rapp MA (2014) Pavlovian-to-instrumental transfer in alcohol dependence: a pilot study. Neuropsychobiology 70:111–121CrossRefPubMedGoogle Scholar
  43. Geisler S, Marinelli M, Degarmo B, Becker ML, Freiman AJ, Beales M, Meredith GE, Zahm DS (2008) Prominent activation of brainstem and pallidal afferents of the ventral tegmental area by cocaine. Neuropsychopharmacology 33:2688–2700CrossRefPubMedPubMedCentralGoogle Scholar
  44. Gerfen CR, Surmeier DJ (2011) Modulation of striatal projection systems by dopamine. Annu Rev Neurosci 34:441–466CrossRefPubMedPubMedCentralGoogle Scholar
  45. Goldberg JA, Ding JB, Surmeier DJ (2012) Muscarinic modulation of striatal function and circuitry. Handb Exp Pharmacol 208:223–241CrossRefPubMedGoogle Scholar
  46. Hall J, Parkinson JA, Connor TM, Dickinson A, Everitt BJ (2001) Involvement of the central nucleus of the amygdala and nucleus accumbens core in mediating Pavlovian influences on instrumental behavior. Eur J Neurosci 13:1984–1992CrossRefPubMedGoogle Scholar
  47. Heimer L, Zahm DS, Churchill L, Kalivas PW, Wohltmann C (1991) Specificity in the projection patterns of acumbal core and shell in the rat. Neuroscience 41:89–125CrossRefPubMedGoogle Scholar
  48. Heinz A, Siessmeier T, Wrase J, Hermann D, Klein S, Grusser S, Flor H, Braus D, Buchholz HG, Grunder G, Schreckenberger M, Smolka M, Rosch F, Mann K, Bartenstein P (2004) Correlation between dopamine D2 receptors in the ventral striatum and central processing of alcohol cues and craving. Am J Psychiatry 161:1783–1789CrossRefPubMedGoogle Scholar
  49. Holland PC (2004) Relations between Pavlovian-instrumental transfer and reinforcer devaluation. J Exp Psychol Anim Behav Process 30:104–117CrossRefPubMedGoogle Scholar
  50. Holland PC, Gallagher M (2003) Double dissociation of the effects of lesion of basolateral and central amygdala on conditioned stimulus-potentiated feeding and Pavlovian-instrumental transfer. Eur J Neurosci 17:1680–1694CrossRefPubMedGoogle Scholar
  51. Holland PC, Rescorla RA (1975) The effect of two ways of devaluing the unconditioned stimulus after first- and second-order appetitive conditioning. J Exp Psychol Anim Behav Process 1:355–363CrossRefGoogle Scholar
  52. Holmes NM, Marchand AR, Coutureau E (2010) Pavlovian to instrumental transfer: a neurobehavioural perspective. Neurosci Biobehav Rev 34:1277–1295CrossRefPubMedGoogle Scholar
  53. Kalivas PW, Churchill L, Romanides A (1999) Involvement of the pallidal-thalamocortical circuit in adaptive behavior. Ann N Y Acad Sci 877:64–70CrossRefPubMedGoogle Scholar
  54. Konorski J (1967) Integrative activity of the brain. University of Chicago Press, ChicagoGoogle Scholar
  55. Kravitz AV, Tye LD, Kreitzer AC (2012) Distinct roles for direct and indirect pathway striatal neurons in reinforcement. Nat Neurosci 15:816–818CrossRefPubMedPubMedCentralGoogle Scholar
  56. Kruse JM, Overmier JB, Konz WA, Rokke E (1983) Pavlovian conditioned stimulus effects upon instrumental choice behavior are reinforcer specific. Learn Motiv 14(2):165–181Google Scholar
  57. Laurent V, Leung B, Maidment N, Balleine BW (2012) Μu- and delta-opioid-related processes in the accumbens core and shell differentially mediate the influence of reward-guided and stimulus-guided decisions on choice. J Neurosci 32:1875–1883CrossRefPubMedPubMedCentralGoogle Scholar
  58. Laurent V, Bertran-Gonzalez J, Chieng BC, Balleine BW (2014) Delta-opioid and dopaminergic processes in accumbens shell modulate the cholinergic control of predictive learning and choice. J Neurosci 34:1358–1369CrossRefPubMedPubMedCentralGoogle Scholar
  59. Laurent V, Wong FL, Balleine BW (2015) δ-opioid receptors in the accumbens shell mediate the influence of both excitatory and inhibitory predictions on choice. Br J Pharmacol 172:562–570CrossRefPubMedPubMedCentralGoogle Scholar
  60. LeBlanc KH, Maidment NT, Ostlund SB (2013) Repeated cocaine exposure facilitates the expression of incentive motivation and induces habitual control in rats. PLoS One 8(4):e61355Google Scholar
  61. Leung BK, Balleine BW (2013) The ventral striato-pallidal pathway mediates the effect of predictive learning on choice between goal-directed actions. J Neurosci 33:13848–13860CrossRefPubMedGoogle Scholar
  62. Leung BK, Balleine BW (2015) Ventral pallidal projections to mediodorsal thalamus and ventral tegmental area play distinct roles in outcome-specific Pavlovian-instrumental transfer. J Neurosci 35:4953–4964CrossRefPubMedGoogle Scholar
  63. Lex A, Hauber W (2008) Dopamine D1 and D2 receptors in the nucleus accumbens core and shell mediate Pavlovian-instrumental transfer. Learn Mem. 15:483–491CrossRefPubMedPubMedCentralGoogle Scholar
  64. Lovibond PF (1983) Facilitation of instrumental behavior by a Pavlovian appetitive conditioned stimulus. J Exp Psychol Anim Behav Process 9:225–247CrossRefPubMedGoogle Scholar
  65. Lu XY, Ghasemzadeh MB, Kalivas PW (1998) Expression of D1 receptor, D2 receptor, substance P and enkephalin messenger RNAs in the neurons projecting from the nucleus accumbens. Neuroscience 82:767–780CrossRefPubMedGoogle Scholar
  66. Mahler SV, Aston-Jones GS (2012) Fos activation of selective afferents to ventral tegmental area during cue-induced reinstatement of cocaine seeking in rats. J Neurosci 32:13026–13309CrossRefGoogle Scholar
  67. Mahler SV, Vazey EM, Beckley JT, Keistler CR, McGlinchey EM, Kaufling J, Wilson SP, Deisseroth K, Woodward JJ, Aston-Jones G (2014) Designer receptors show role for ventral pallidum input to ventral tegmental area in cocaine seeking. Nat Neurosci 17:577–585CrossRefPubMedPubMedCentralGoogle Scholar
  68. Martinovic J, Jones A, Christiansen P, Rose AK, Hogarth L, Field M (2014) Electrophysiological responses to alcohol cues are not associated with Pavlovian-to-instrumental transfer in social drinkers. PLoS One 9(4):e94605Google Scholar
  69. McAlonan GM, Robbins TW, Everitt BJ (1993) Effects of medial dorsal thalamic and ventral pallidal lesions on the acquisition of a conditioned place preference: further evidence for the involvement of the ventral striatopallidal system in reward-related processes. Neuroscience 52:605–620CrossRefPubMedGoogle Scholar
  70. Mink JW (1996) The basal ganglia: focused selection and inhibition of competing motor programs. Prog Neurobiol 50:381–425CrossRefPubMedGoogle Scholar
  71. Mogenson GJ, Jones DL, Yim CY (1980) From motivation to action: functional interface between the limbic system and the motor system. Prog Neurobiol 14:69–97CrossRefPubMedGoogle Scholar
  72. Morgado P, Silva M, Sousa N, Cerqueira JJ (2012) Stress transiently affects Pavlovian-to-instrumental transfer. Front Neurosci 6:93Google Scholar
  73. Mowrer OH (1960) Learning theory and behavior, Wiley, New YorkGoogle Scholar
  74. Nelson A, Killcross S (2006) Amphetamine exposure enhances habit formation. J Neurosci 26:3805–3812CrossRefPubMedGoogle Scholar
  75. Murschall A, Hauber W (2006) Inactivation of the ventral tegmental area abolished the general excitatory influence of Pavlovian cues on instrumental performance. Learn Mem 13:123–126CrossRefPubMedGoogle Scholar
  76. Ostlund SB, Balleine BW (2007) Instrumental reinstatement depends on sensory- and motivationally-specific features of the instrumental outcome. Learn Behav 35(1):43–52CrossRefPubMedGoogle Scholar
  77. Ostlund SB, Balleine BW (2008) Differential involvement of the basolateral amygdala and mediodorsal thalamus in instrumental action selection. J Neurosci 28:4398–4405CrossRefPubMedPubMedCentralGoogle Scholar
  78. Ostlund SB, Maidment NT (2012) Dopamine receptor blockade attenuates the general incentive motivational effects of noncontingently delivered rewards and reward-paired cues without affecting their ability to bias action selection. Neuropsychopharmacology 37:508–519CrossRefPubMedPubMedCentralGoogle Scholar
  79. Overmier JB, Lawry JA (1979) Pavlovian conditioning and the mediation of behavior. Psychology of Learning and Motivation 13:1–55Google Scholar
  80. Pavlov IP (1927) Conditioned reflexes. Oxford University Press, Oxford, UKGoogle Scholar
  81. Parnaudeau S, Taylor K, Bolkan SS, Ward RD, Balsam PD, Kellendonk C (2015) Mediodorsal thalamus hypofunction impairs flexible goal-directed behavior. Biol Psychiatry 77:445–453CrossRefPubMedPubMedCentralGoogle Scholar
  82. Peciña S, Schulkin J, Berridge KC (2006) Nucleus accumbens corticotropin-releasing factor increases cue-triggered motivation for sucrose reward: paradoxical positive incentive effects in stress? BMC Biol 4:8Google Scholar
  83. Peciña S, Berridge KC (2013) Dopamine or opioid stimulation of nucleus accumbens similarly amplify cue‐triggered ‘wanting’ for reward: entire core and medial shell mapped as substrates for PIT enhancement. Eur J Neurosci 37(9):1529–1540Google Scholar
  84. Pielock SM, Lex B, Hauber W (2011) The role of dopamine in the dorsomedial striatum in general and outcome-selective Pavlovian-instrumental transfer. Eur J Neurosci 33:717–725CrossRefPubMedGoogle Scholar
  85. Pool E, Brosch T, Delplanque S, Sander D (2015) Stress increases cue-triggered “wanting” for sweet reward in humans. J Exp Psychol Anim Learn Cogn 41:128–136CrossRefPubMedGoogle Scholar
  86. Ray OS, Stein L (1959) Generalization of conditioned suppression. J Exp Anal Behav 2:357–361CrossRefPubMedPubMedCentralGoogle Scholar
  87. Rescorla RA (1994) Transfer of instrumental control mediated by a devalued outcome. Anim Learn Behav 22:27–33CrossRefGoogle Scholar
  88. Rescorla RA, LoLordo VM (1965) Inhibition of avoidance behavior. J Comp Physiol Psychol 59:406–412CrossRefPubMedGoogle Scholar
  89. Rescorla RA, Solomon RL (1967) Two-process learning theory: relationship between Pavlovian conditioning and instrumental learning. Psychol Rev 74:151–182CrossRefPubMedGoogle Scholar
  90. Saddoris MP, Stamatakis A, Carelli RM (2011) Neural correlates of Pavlovian-to-instrumental transfer in the nucleus accumbens shell are selectively potentiated following cocaine self-administration. Eur J Neurosci 33:2274–2287CrossRefPubMedGoogle Scholar
  91. Salamone JD, Correa M, Farrar A, Mingote SM (2007) Effort-related functions of nucleus accumbens dopamine and associated forebrain circuits. Psychopharmacology 191:461–482CrossRefPubMedGoogle Scholar
  92. Scherrer G, Tryoen-Tóth P, Filliol D, Matifas A, Laustriat D, Cao YQ, Basbaum AI, Dierich A, Vonesh JL, Gavériaux-Ruff C, Kieffer BL (2006) Knockin mice expressing fluorescent delta-opioid receptors uncover G protein-coupled receptor dynamics in vivo. Proc Natl Acad Sci 103:9691–9696CrossRefPubMedPubMedCentralGoogle Scholar
  93. Schwabe L, Wolf OT (2010) Socially evaluated cold pressor stress after instrumental learning favors habits over goal-directed action. Psychoneuroendocrinology. 35:977–986CrossRefPubMedGoogle Scholar
  94. Schultz W (2006) Behavioral theories and the neurophysiology of reward. Annu Rev Psychol 2006(57):87–115CrossRefGoogle Scholar
  95. Shiflett MW (2012) The effects of amphetamine exposure on outcome-selective Pavlovian-instrumental transfer in rats. Psychopharmacology 223(3):361–370CrossRefPubMedPubMedCentralGoogle Scholar
  96. Shiflett MW, Balleine BW (2010) At the limbic-motor interface: disconnection of basolateral amygdala from nucleus accumbens core and shell reveals dissociable components of incentive motivation. Eur J Neurosci 32:1735–1743CrossRefPubMedPubMedCentralGoogle Scholar
  97. Smith RJ, Lobo MK, Spencer S, Kalivas PW (2013) Cocaine-induced adaptations in D1 and D2 accumbens projection neurons (a dichotomy not necessarily synonymous with direct and indirect pathways). Curr Opin Neurobiol 23:546–552CrossRefPubMedPubMedCentralGoogle Scholar
  98. Soares-Cunha C, Coimbra B, Borges S, Carvalho MM, Rodrigues AJ, Sousa N (2014) The motivational drive to natural rewards is modulated by prenatal glucocorticoid exposure. Transl Psychiatry. 2014(4):e397CrossRefGoogle Scholar
  99. Solomon RL, Turner LH (1962) Discriminative classical conditioning in dogs paralyzed by curare can later control discriminative discriminative avoidance responses in the normal state. Psychol Rev 69:202–219CrossRefPubMedGoogle Scholar
  100. Stocco A (2012) Acetylcholine-based entropy in response selection: a model of how striatal interneurons modulate exploration, exploitation, and response variability in decision-making. Front Neurosci 6:18CrossRefPubMedPubMedCentralGoogle Scholar
  101. Toates FM (1986) Motivational systems. Cambridge University Press, CambridgeGoogle Scholar
  102. Trapold MA, Overmier JB (1972) The second learning process in instrumental learning. In: Black AA, Prokasy WF (eds) Classical conditioning II: current research and theory. Appleton-Century-Crofts, New York, pp 427–452Google Scholar
  103. Tripathi A, Prensa L, Mengual E (2013) Axonal branching patterns of ventral pallidal neurons in the rat. Brain Struct Funct 218:1133–1157CrossRefPubMedGoogle Scholar
  104. Vanderschuren LJ, Di Ciano P, Everitt BJ (2005) Involvement of the dorsal striatum in cue-controlled cocaine seeking. J Neurosci 25:8665–8670CrossRefPubMedGoogle Scholar
  105. Wassum KM, Ostlund SB, Loewinger GC, Maidment NT (2013) Phasic mesolimbic dopamine release tracks reward seeking during expression of Pavlovian-to-instrumental transfer. Biol Psychiatry 73(8):747–755CrossRefPubMedPubMedCentralGoogle Scholar
  106. Watson P, Wiers RW, Hommel B, de Wit S (2014) Working for food you don’t desire cues interfere with goal-directed food-seeking. Appetite 79:139–148CrossRefPubMedGoogle Scholar
  107. Wiers CE, Stelzel C, Park SQ, Gawron CK, Ludwig VU, Gutwinski S, Heinz A, Lindenmeyer J, Wiers RW, Walter H, Bermpohl F (2014) Neural correlates of alcohol-approach bias in alcohol addiction: the spirit is willing but the flesh is weak for spirits. Neuropsychopharmacology 39:688–697CrossRefPubMedPubMedCentralGoogle Scholar
  108. Winterbauer NE, Balleine BW (2005) Motivational control of second-order conditioning. J Exp Psychol Anim Behav Process 31(3):334–340CrossRefPubMedGoogle Scholar
  109. Wyvell CL, Berridge KC (2000) Intra-accumbens amphetamine increases the conditioned incentive salience of sucrose reward: enhancement of reward “wanting” without enhanced “liking” or response reinforcement. J Neurosci 20:8122–8130PubMedGoogle Scholar
  110. Wyvell CL, Berridge KC (2001) Incentive sensitization by previous amphetamine exposure: increased cue-triggered “wanting” for sucrose reward. J Neurosci 21:7831–7840PubMedGoogle Scholar
  111. Yin HH, Ostlund SB, Knowlton BJ, Balleine BW (2005) The role of the dorsomedial striatum in instrumental conditioning. Eur J Neurosci 22:513–523CrossRefPubMedGoogle Scholar
  112. Zahm DS (2000) An integrative neuroanatomical perspective on some subcortical substrates of adaptive responding with emphasis on the nucleus accumbens. Neurosci Biobehav Rev 24:85–105CrossRefPubMedGoogle Scholar
  113. Zahm DS, Heimer L (1990) Two transpallidal pathways originating in the rat nucleus accumbens. J Comp Neurol 302:437–446CrossRefPubMedGoogle Scholar
  114. Zener K (1937) The significance of behavior accompanying conditioned salivary secretion for theories of the conditioned response. Am J Psychol 50:384–403CrossRefGoogle Scholar
  115. Zhou L, Furuta T, Kaneko T (2003) Chemical organization of projection neurons in the rat accumbens nucleus and olfactory tubercle. Neuroscience 120:783–798CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  1. 1.Department of PsychologyUniversity of SydneySydneyAustralia
  2. 2.Brain and Mind Research InstituteUniversity of SydneyCamperdownAustralia

Personalised recommendations