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Cited by 1,450Neurotransmitter Receptor Influence on BehaviorNeural and Behavioral Psychology StudiesMemory and Neural Mechanisms

The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking

Ikemoto, Satoshi, Panksepp, Jaak·1999·Brain Research Reviews
DOI 10.1016/s0165-0173(99)00023-5
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Abstract

Studies addressing behavioral functions of dopamine (DA) in the nucleus accumbens septi (NAS) are reviewed. A role of NAS DA in reward has long been suggested. However, some investigators have questioned the role of NAS DA in rewarding effects because of its role in aversive contexts. As findings supporting the role of NAS DA in mediating aversively motivated behaviors accumulate, it is necessary to accommodate such data for understanding the role of NAS DA in behavior. The aim of the present paper is to provide a unifying interpretation that can account for the functions of NAS DA in a variety of behavioral contexts: (1) its role in appetitive behavioral arousal, (2) its role as a facilitator as well as an inducer of reward processes, and (3) its presently undefined role in aversive contexts. The present analysis suggests that NAS DA plays an important role in sensorimotor integrations that facilitate flexible approach responses. Flexible approach responses are contrasted with fixed instrumental approach responses (habits), which may involve the nigro-striatal DA system more than the meso-accumbens DA system. Functional properties of NAS DA transmission are considered in two stages: unconditioned behavioral invigoration effects and incentive learning effects. (1) When organisms are presented with salient stimuli (e.g., novel stimuli and incentive stimuli), NAS DA is released and invigorates flexible approach responses (invigoration effects). (2) When proximal exteroceptive receptors are stimulated by unconditioned stimuli, NAS DA is released and enables stimulus representations to acquire incentive properties within specific environmental context. It is important to make a distinction that NAS DA is a critical component for the conditional formation of incentive representations but not the retrieval of incentive stimuli or behavioral expressions based on over-learned incentive responses (i.e., habits). Nor is NAS DA essential for the cognitive perception of environmental stimuli. Therefore, even without normal NAS DA transmission, the habit response system still allows animals to perform instrumental responses given that the tasks take place in fixed environment. Such a role of NAS DA as an incentive-property constructor is not limited to appetitive contexts but also aversive contexts. This dual action of NAS DA in invigoration and incentive learning may explain the rewarding effects of NAS DA as well as other effects of NAS DA in a variety of contexts including avoidance and unconditioned/conditioned increases in open-field locomotor activity. Particularly, the present hypothesis offers the following interpretation for the finding that both conditioned and unconditioned aversive stimuli stimulate DA release in the NAS: NAS DA invigorates approach responses toward 'safety'. Moreover, NAS DA modulates incentive properties of the environment so that organisms emit approach responses toward 'safety' (i.e., avoidance responses) when animals later encounter similar environmental contexts. There may be no obligatory relationship between NAS DA release and positive subjective effects, even though these systems probably interact with other brain systems which can mediate such effects. The present conceptual framework may be valuable in understanding the dynamic interplay of NAS DA neurochemistry and behavior, both normal and pathophysiological.

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317 of 317 references verified0 citation errors · 0 not checkable

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  • Reward-related mesolimbic dopamine steers animal behavior, creating automatic approach toward reward-associated objects and avoidance of objects unlikely to be beneficial.

    “Reward-related mesolimbic dopamine steers animal behavior, creating automatic approach toward reward-associated objects and avoidance of objects unlikely to be beneficial.”

    From Reward Changes Salience in Human Vision via the Anterior Cingulate (2010) · cites this paper as Ikemoto and Panksepp, 1999

  • Theories of the function of dopamine in reinforcement learning and animal approach behavior place reward firmly at the center of attentional control.

    “theories of the function of dopamine in reinforcement learning and animal approach behavior place reward firmly at the center of attentional control (Berridge and Robinson, 1998; Ikemoto and Panksepp, 1999; Redgrave et al., 1999; Wise, 2004; Alcaro et al., 2007).”

    From Reward Changes Salience in Human Vision via the Anterior Cingulate (2010) · cites this paper as Ikemoto and Panksepp, 1999

  • The mesolimbic dopamine pathway is generally thought to be involved in motivation to work for rewards and in the salience of incentives.

    “the mesolimbic DA pathway is generally thought to be involved in both the motivation to act or work for rewards, and the salience of incentives (Mogenson 1987; Blackburn et al 1992; Ikemoto and Panksepp 1999; for a complete discussion of the many competing theories regarding the role of the mesolimbic DA pathway, see Wise 2004; Berridge 2007).”

    From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Ikemoto and Panksepp 1999

  • Nucleus accumbens dopamine has been implicated in two major roles: invigoration of approach and incentive learning.

    “Nucleus accumbens dopamine has been implicated in two major roles: invigoration of approach and incentive learning* (Ikemoto and Panksepp, 1999).”

    From Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex (2007) · cites this paper as Ikemoto and Panksepp, 1999

  • Dopamine in the accumbens plays an important role in incentive learning, particularly with the presence of incentive stimuli.

    “In addition to such energizing effects, particularly with the presence of incentive stimuli*, dopamine in the accumbens plays an important role in incentive learning (Ikemoto and Panksepp, 1999).”

    From Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex (2007) · cites this paper as Ikemoto and Panksepp, 1999

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Authors
Ikemoto, S., & Panksepp, J.
Affiliations
  • National Institute on Drug Abuse (US)
  • Bowling Green State University (US)
Corresponding author
Ikemoto, Satoshi
ORCID
Ikemoto, Satoshi
Venue
Brain Research Reviews
Publisher
Elsevier BV
Published
1999-12
Volume
31
Issue
1
Pages
6-41
ISSN
0165-0173 (ISSN-L)
DOI
10.1016/s0165-0173(99)00023-5
OpenAlex
W1968490092
Cited by
1,450
References
317
Citations by year
2026: 15 · 2025: 31 · 2024: 35 · 2023: 37 · 2022: 50 · 2021: 43 · 2020: 83 · 2019: 52 · 2018: 49 · 2017: 53 · 2016: 53 · 2015: 59 · 2014: 86 · 2013: 68 · 2012: 84
FWCI
2.92
Type
journal article
Language
en
Open access
closed
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Brain Research Reviews (publishedVersion)
  • PubMed (publishedVersion)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords
nucleus accumbens septi, dopamine, reward seeking, aversive motivation, incentive learning, habit formation, sensorimotor integration, avoidance behavior, locomotor activity, approach-avoidance behavior, incentive salience
MeSH terms
Animals, Behavior, Behavior, Animal, Dopamine, Humans, Motivation, Nucleus Accumbens, Reward, Rats

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