Skip to main content

Part of the book series: Current Topics in Behavioral Neurosciences ((CTBN,volume 37))

Abstract

Data from experimental animals and human subjects has provided convergent evidence for the key role of the striatum in the formation of stimulus-response habits. Habits can be distinguished from associative memories that support goal-directed actions based on their insensitivity to reward devaluation and contingency degradation. Behavior on many instrumental learning tasks can be supported by both declarative knowledge and habits, and these contributions shift with the amount of training. This shift appears to be accompanied by the involvement of different cortico-striatal loops in controlling behavior. Factors that encourage the shift toward and maintenance of habits include learning under conditions of stress, distraction, and interval or probabilistic schedules of reinforcement.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adams CD (1982) Variations in the sensitivity of instrumental responding to reinforcer devaluation. Q J Exp Psychol Sect B 34B(2):77–98

    Article  Google Scholar 

  • Adams CD, Dickinson A (1981) Instrumental responding following reinforcer devaluation. Q J Exp Psychol Sect B 33B(2):109–121

    Article  Google Scholar 

  • Alexander GE, DeLong MR, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9:357–381

    Article  CAS  PubMed  Google Scholar 

  • Balleine BW (2001) Incentive processes in instrumental conditioning. In: Handbook of contemporary learning theories, Psychology Press, USA, pp 307–366

    Google Scholar 

  • Balleine BW, Dickinson A (1998a) Goal-directed instrumental action: contingency and incentive learning and their cortical substrates. Neuropharmacology 37(4–5):407–419

    Article  CAS  PubMed  Google Scholar 

  • Balleine BW, Dickinson A (1998b) The role of incentive learning in instrumental outcome revaluation by sensory-specific satiety. Learn Behav 26(1):46–59

    Article  Google Scholar 

  • Bayley PJ, Frascino JC, Squire LR (2005) Robust habit learning in the absence of awareness and independent of the medial temporal lobe. Nature 436(7050):550–553

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Belin D, Jonkman S, Dickinson A, Robbins TW, Everitt BJ (2009) Parallel and interactive learning processes within the basal ganglia: Relevance for the understanding of addiction. Behav Brain Res 199(1):89–102

    Article  PubMed  Google Scholar 

  • Bohbot VD, Iaria G, Petrides M (2004) Hippocampal function and spatial memory: evidence from functional neuroimaging in healthy participants and performance of patients with medial temporal lobe resections. Neuropsychology 18(3):418–425

    Article  PubMed  Google Scholar 

  • Bohbot VD, Lerch J, Thorndycraft B, Iaria G, Zijdenbos AP (2007) Gray matter differences correlate with spontaneous strategies in a human virtual navigation task. J Neurosci 27(38):10078–10083

    Article  CAS  PubMed  Google Scholar 

  • Capaldi EJ (1966) Partial reinforcement: a hypothesis of sequential effects. Psychol Rev 73(5):459–477

    Article  CAS  PubMed  Google Scholar 

  • Capaldi EJ (1967) A sequential hypothesis of instrumental learning. In: Spence KW, Spence JT (eds) The psychology of learning and motivation: advances in research and theory, vol 1. Academic Press, New York, pp 67–156

    Google Scholar 

  • Chang Q, Gold PE (2003) Intra-hippocampal lidocaine injections impair acquisition of a place task and facilitate acquisition of a response task in rats. Behav Brain Res 144(1–2):19–24

    Article  CAS  PubMed  Google Scholar 

  • Colwill RM, Rescorla RA (1985) Postconditioning devaluation of a reinforcer affects instrumental responding. J Exp Psychol: Anim Behav Processes 11(1):120–132

    Google Scholar 

  • 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(5940):621–625

    Article  CAS  PubMed  Google Scholar 

  • Dickinson A (1985) Actions and habits: the development of behavioural autonomy. Philos Trans R Soc Lond Ser B: Biol Sci 308(1135):67–78

    Article  Google Scholar 

  • Dickinson A, Nicholas DJ, Adams CD (1983) The effect of the instrumental training contingency on susceptibility to reinforcer devaluation. Q J Exp Psychol Sect B-Comp Physiol Psychol 35(FEB):35–51

    Article  Google Scholar 

  • Dube SR, Felitti VJ, Dong M, Chapman DP, Giles WH, Anda RF (2003a) Childhood abuse, neglect, and household dysfunction and the risk of illicit drug use: the adverse childhood experiences study. Pediatrics 111(3):564–572

    Article  PubMed  Google Scholar 

  • Dube SR, Felitti VJ, Dong M, Giles WH, Anda RF (2003b) The impact of adverse childhood experiences on health problems: evidence from four birth cohorts dating back to 1900. Prev Med 37(3):268–277

    Article  PubMed  Google Scholar 

  • Everitt BJ, Robbins TW (2005) Neural systems of reinforcement for drug addiction: From actions to habits to compulsion. Nat Neurosci 8(11):1481–1489

    Article  CAS  PubMed  Google Scholar 

  • Fernandez-Ruiz J, Wang J, Aigner TG, Mishkin N (2001) Visual habit formation in monkeys with neurotoxic lesions of the ventrocaudal neostriatum. Proc Natl Acad Sci USA 98(7):4196–4201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferragud A, Haro A, Sylvain A, Velazquez-Sanchez C, Hernandez-Rabaza V, Canales JJ (2010) Enhanced habit-based learning and decreased neurogenesis in the adult hippocampus in a murine model of chronic social stress. Behav Brain Res 210(1):134–139

    Article  CAS  PubMed  Google Scholar 

  • Foerde K, Shohamy D (2011) The role of the basal ganglia in learning and memory: Insight from parkinson’s disease. Neurobiol Learn Mem 96(4):624–636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foerde K, Knowlton BJ, Poldrack RA (2006) Modulation of competing memory systems by distraction. Proc Natl Acad Sci USA 103(31):11778–11783

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foerde K, Poldrack RA, Knowlton BJ (2007) Secondary-task effects on classification learning. Mem Cognition 35(5):864–874

    Article  Google Scholar 

  • Gee DG, Gabard-Durnam LJ, Flannery J, Goff B, Humphreys KL, Telzer EH, Hare TA, Bookheimer SY, Tottenham N (2013) Early developmental emergence of human amygdala-prefrontal connectivity after maternal deprivation. Proc Natl Acad Sci USA 110(39):15638–15643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gillan CM, Morein-Zamir S, Urcelay GP, Sule A, Voon V, Apergis-Schoute AM, Fineberg NA, Sahakian BJ, Robbins TW (2014) Enhanced avoidance habits in obsessive-compulsive disorder. Biol Psychiatry 75(8):631–638

    Article  PubMed  PubMed Central  Google Scholar 

  • Gillan CM, Apergis-Schoute AM, Morein-Zamir S, Urcelay GP, Sule A, Fineberg NA, Sahakian BJ, Robbins TW (2015) Functional neuroimaging of avoidance habits in obsessive-compulsive disorder. Am J Psychiatry 172(3):284–293

    Article  PubMed  Google Scholar 

  • Grissom EM, Hawley WR, Bromley-Dulfano SS, Marino SE, Stathopoulos NG, Dohanich GP (2012) Learning strategy is influenced by trait anxiety and early rearing conditions in prepubertal male, but not prepubertal female rats. Neurobiol Learn Mem 98(2):174–181

    Article  PubMed  Google Scholar 

  • 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 behaviour. Eur J Neurosci 13(10):1984–1992

    Article  CAS  PubMed  Google Scholar 

  • Hull CL (1943) Principles of behavior. Appleton-Century-Crofts, New York

    Google Scholar 

  • Iaria G, Petrides M, Dagher A, Pike B, Bohbot VD (2003) Cognitive strategies dependent on the hippocampus and caudate nucleus in human navigation: Variability and change with practice. J Neurosci 23(13):5945–5952

    CAS  PubMed  Google Scholar 

  • Joels M, Karst H, Krugers HJ, Lucassen PJ (2007) Chronic stress: implications for neuronal morphology, function and neurogenesis. Front Neuroendocrin 28(2–3):72–96

    Article  Google Scholar 

  • Killcross S, Coutureau E (2003) Coordination of actions and habits in the medial prefrontal cortex of rats. Cereb Cortex 13(4):400–408

    Article  PubMed  Google Scholar 

  • Kim JJ, Lee HJ, Han J-S, Packard MG (2001) Amygdala is critical for stress-induced modulation of hippocampal long-term potentiation and learning. J Neurosci 21(14):5222–5238

    CAS  PubMed  Google Scholar 

  • Knowlton BJ (2002) The role of the basal ganglia in learning and memory. In: Squire LR, Schacter DL (eds) Neuropsychology of memory, 3rd edn. Guilford Press, New York, pp 143–153

    Google Scholar 

  • Knowlton BJ, Moody TD (2008) Procedural learning in humans. In: Byrne JH (ed) Learning and memory: a comprehensive reference: Vol 3 memory systems. Academic Press, Oxford, pp 321–340

    Chapter  Google Scholar 

  • Knowlton BJ, Squire LR, Gluck MA (1994) Probabilistic classification learning in amnesia. Learn Memory 1(2):106–120

    CAS  Google Scholar 

  • Knowlton BJ, Mangels JA, Squire LR (1996) A neostriatal habit learning system in humans. Science 273(5280):1399–1402

    Article  CAS  PubMed  Google Scholar 

  • Lovibond PF (1983) Facilitation of instrumental behavior by a pavlovian appetitive conditioned-stimulus. J Exp Psychol-Anim Behav Process 9(3):225–247

    Article  CAS  PubMed  Google Scholar 

  • Ludwig AM, Wikler A, Stark LH (1974) The first drink: Psychobiological aspects of craving. Arch Gen Psychiatry 30(4):539–547

    Article  CAS  PubMed  Google Scholar 

  • Lupien SJ, McEwen BS, Gunnar MR, Heim C (2009) Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 10(6):434–445

    Article  CAS  PubMed  Google Scholar 

  • Macleod J, Hickman M, Jones HE, Copeland L, McKenzie J, De Angelis D, Kimber J, Robertson JR (2013) Early life influences on the risk of injecting drug use: case control study based on the edinburgh addiction cohort. Addiction 108(4):743–750

    Article  PubMed  Google Scholar 

  • McDonald RJ, White NM (1994) Parallel information processing in the water maze: evidence for independent memory systems involving dorsal striatum and hippocampus. Behav Neural Biol 61(3):260–270

    Article  CAS  PubMed  Google Scholar 

  • McEwen BS (2000) Effects of adverse experiences for brain structure and function. Biol Psychiatry 48(8):721–731

    Article  CAS  PubMed  Google Scholar 

  • McEwen BS (2003) Early life influences on life-long patterns of behavior and health. Mental Retard Dev Disabil Res Rev 9(3):149–154

    Article  Google Scholar 

  • Milner B (1962) Les troubles de la memoire accompagnant les lesions hippocampiques bilaterales. In: Passouant P (ed) Physiologie de l’hippocampe. Centre National de la Recherche Scientifique, Paris, pp 257–272

    Google Scholar 

  • Moody TD, Bookheimer SY, Vanek Z, Knowlton BJ (2004) An implicit learning task activates medial temporal lobe in patients with parkinson’s disease. Behav Neurosci 118(2):438–442

    Article  PubMed  Google Scholar 

  • Moody TD, Chang GY, Vanek ZF, Knowlton BJ (2010) Concurrent discrimination learning in parkinson’s disease. Behav Neurosci 124(1):1–8

    Article  PubMed  Google Scholar 

  • Mowrer OH, Jones H (1945) Habit strength as a function of the pattern of reinforcement. J Exp Psychol 35(4):293–311

    Article  Google Scholar 

  • Neal DT, Wood W, Wu M, Kurlander D (2011) The pull of the past: when do habits persist despite conflict with motives? Pers Soc Psychol Bull 37(11):1428–1437

    Article  PubMed  Google Scholar 

  • Packard MG (2009a) Anxiety, cognition, and habit: a multiple memory systems perspective. Brain Res 1293:121–128

    Article  CAS  PubMed  Google Scholar 

  • Packard MG (2009b) Exhumed from thought: Basal ganglia and response learning in the plus-maze. Behav Brain Res 199(1):24–31

    Article  PubMed  Google Scholar 

  • Packard MG, Goodman J (2012) Emotional arousal and multiple memory systems in the mammalian brain. Front Behav Neurosci 6:14

    Article  PubMed  PubMed Central  Google Scholar 

  • Packard MG, Knowlton BJ (2002) Learning and memory functions of the basal ganglia. Annu Rev Neurosci 25(1):563–593

    Article  CAS  PubMed  Google Scholar 

  • Packard MG, McGaugh JL (1992) Double dissociation of fornix and caudate-nucleus lesions on acquisition of 2 water maze tasks: Further evidence for multiple memory systems. Behav Neurosci 106(3):439–446

    Article  CAS  PubMed  Google Scholar 

  • Packard MG, McGaugh JL (1996) Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiol Learn Mem 65(1):65–72

    Article  CAS  PubMed  Google Scholar 

  • Packard MG, Hirsh R, White NM (1989) Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: Evidence for multiple memory systems. J Neurosci 9(5):1465–1472

    CAS  PubMed  Google Scholar 

  • Patterson TK, Craske MG, Knowlton BJ (2013) The effect of early-life stress on memory systems supporting instrumental behavior. Hippocampus 23(11):1025–1034

    Article  PubMed  Google Scholar 

  • Poldrack RA, Packard MG (2003) Competition among multiple memory systems: converging evidence from animal and human brain studies. Neuropsychologia 41(3):245–251

    Article  PubMed  Google Scholar 

  • Poldrack RA, Prabhakaran V, Seger CA, Gabrieli JDE (1999) Striatal activation during acquisition of a cognitive skill. Neuropsychology 13(4):564–574

    Article  CAS  PubMed  Google Scholar 

  • Poldrack RA, Clark J, Pare-Blagoev EJ, Shohamy D, Creso Moyano J, Myers C, Gluck MA (2001) Interactive memory systems in the human brain. Nature 414(6863):546–550

    Article  CAS  PubMed  Google Scholar 

  • Rescorla RA, Solomon RL (1967) 2-process learning theory—relationships between pavlovian conditioning and instrumental learning. Psychol Rev 74(3):151

    Article  CAS  PubMed  Google Scholar 

  • Sage JR, Knowlton BJ (2000) Effects of us devaluation on win-stay and win-shift radial maze performance in rats. Behav Neurosci 114(2):295–306

    Article  CAS  PubMed  Google Scholar 

  • Schroeder JP, Wingard JC, Packard MG (2002) Post-training reversible inactivation of hippocampus reveals interference between memory systems. Hippocampus 12(2):280–284

    Article  PubMed  Google Scholar 

  • Schwabe L, Wolf OT (2009) Stress prompts habit behavior in humans. J Neurosci 29(22):7191–7198

    Article  CAS  PubMed  Google Scholar 

  • Schwabe L, Wolf OT (2010) Socially evaluated cold pressor stress after instrumental learning favors habits over goal-directed action. Psychoneuroendocrinology 35(7):977–986

    Article  PubMed  Google Scholar 

  • Schwabe L, Wolf OT (2011) Stress-induced modulation of instrumental behavior: From goal-directed to habitual control of action. Behav Brain Res 219(2):321–328

    Article  PubMed  Google Scholar 

  • Schwabe L, Oitzl MS, Philippsen C, Richter S, Bohringer A, Wippich W, Schachinger H (2007) Stress modulates the use of spatial versus stimulus-response learning strategies in humans. Learn Mem 14(1):109–116

    Article  PubMed  PubMed Central  Google Scholar 

  • Schwabe L, Dalm S, Schachinger H, Oitzl MS (2008) Chronic stress modulates the use of spatial and stimulus-response learning strategies in mice and man. Neurobiol Learn Mem 90(3):495–503

    Article  PubMed  Google Scholar 

  • Schwabe L, Dickinson A, Wolf OT (2011) Stress, habits, and drug addiction: a psychoneuroendocrinological perspective. Exp Clin Psychopharmacol 19(1):53–63

    Article  PubMed  Google Scholar 

  • Schwabe L, Bohbot VD, Wolf OT (2012) Prenatal stress changes learning strategies in adulthood. Hippocampus 22(11):2136–2143

    Article  PubMed  Google Scholar 

  • Soares JM, Sampaio A, Ferreira LM, Santos NC, Marques F, Palha JA, Cerqueira JJ, Sousa N (2012) Stress-induced changes in human decision-making are reversible. Transl Psychiatry 2:e131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teng E, Stefanacci L, Squire LR, Zola SM (2000) Contrasting effects on discrimination learning after hippocampal lesions and conjoint hippocampal-caudate lesions in monkeys. J Neurosci 20(10):3853–3863

    CAS  PubMed  Google Scholar 

  • Tolman EC (1932) Purposive behavior in animals and men. Century, New York

    Google Scholar 

  • Tolman EC, Ritchie BF, Kalish D (1946) Studies in spatial learning: 2. Place learning versus response learning. J Exp Psychol 36(3):221–229

    Article  CAS  PubMed  Google Scholar 

  • Tottenham N (2014) The importance of early experiences for neuro-affective development. In: Andersen SL, Pine DS (eds) Current topics in behavioral neurosciences: Vol 16 the neurobiology of childhood. Springer, New York, pp 109–129

    Google Scholar 

  • Tottenham N, Sheridan MA (2009) A review of adversity, the amygdala and the hippocampus: A consideration of developmental timing. Front Hum Neurosci 3:68

    PubMed  Google Scholar 

  • Tottenham N, Hare TA, Quinn BT, McCarry TW, Nurse M, Gilhooly T, Millner A, Galvan A, Davidson MC, Eigsti IM et al (2010) Prolonged institutional rearing is associated with atypically large amygdala volume and difficulties in emotion regulation. Dev Sci 13(1):46–61

    Article  PubMed  PubMed Central  Google Scholar 

  • Tricomi EM, Delgado MR, Fiez JA (2004) Modulation of caudate activity by action contingency. Neuron 41(2):281–292

    Article  CAS  PubMed  Google Scholar 

  • Tricomi E, Balleine BW, O’Doherty JP (2009) A specific role for posterior dorsolateral striatum in human habit learning. Eur J Neurosci 29(11):2225–2232

    Article  PubMed  PubMed Central  Google Scholar 

  • Valentin VV, Dickinson A, O’Doherty JP (2007) Determining the neural substrates of goal-directed learning in the human brain. J Neurosci 27(15):4019–4026

    Article  CAS  PubMed  Google Scholar 

  • Vogel-Sprott M (1967) Partial-reward training for resistance to punishment and to subsequent extinction. J Exp Psychol 75(1):138–140

    Article  CAS  PubMed  Google Scholar 

  • Yin HH, Knowlton BJ (2004) Contributions of striatal subregions to place and response learning. Learn Memory 11(4):459–463

    Article  Google Scholar 

  • Yin HH, Knowlton BJ (2006) The role of the basal ganglia in habit formation. Nat Rev Neurosci 7(6):464–476

    Article  CAS  PubMed  Google Scholar 

  • Yin HH, Knowlton BJ, Balleine BW (2004) Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning. Eur J Neurosci 19(1):181–189

    Article  PubMed  Google Scholar 

  • Yin HH, Ostlund SB, Knowlton BJ, Balleine BW (2005) The role of the dorsomedial striatum in instrumental conditioning. Eur J Neurosci 22(2):513–523

    Article  PubMed  Google Scholar 

  • Yin HH, Knowlton BJ, Balleine BW (2006) Inactivation of dorsolateral striatum enhances sensitivity to changes in the action–outcome contingency in instrumental conditioning. Behav Brain Res 166(2):189–196

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Barbara J. Knowlton .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Knowlton, B.J., Patterson, T.K. (2016). Habit Formation and the Striatum. In: Clark, R.E., Martin, S. (eds) Behavioral Neuroscience of Learning and Memory. Current Topics in Behavioral Neurosciences, vol 37. Springer, Cham. https://doi.org/10.1007/7854_2016_451

Download citation

Publish with us

Policies and ethics