Taste reactivity analysis of 6-hydroxydopamine-induced aphagia: Implications for arousal and anhedonia hypotheses of dopamine function.
Abstract
The deficits in feeding and drinking that result from 6-hydroxydopamine (6-OHDA) lesions of the mesostriatal dopamine system are often explained using either sensorimotor arousal or anhedonia hypotheses. Sensorimotor arousal hypotheses posit that dopamine systems facilitate the capacity of sensory stimuli to activate any motor output. The anhedonia hypothesis suggests that dopamine systems amplify the hedonic impact of positive reinforcers. Natural palatability-dependent ingestive and aversive actions, which are emitted by rats to tastes, provide a sensitive test that can discriminate between these hypotheses: A reduction of sensorimotor arousal should diminish the ability of tastes to elicit any actions, whereas anhedonia should shift the balance between positive and aversive actions. To directly compare these two hypotheses, taste reactivity was examined in rats made aphagic by intranigral 6-OHDA injections. The results did not support either of these predictions: Taste reactivity was essentially unchanged. The persistence of normal taste reactivity argues against both an anhedonia and a global sensorimotor arousal interpretation and provides further evidence that the capacity for hedonics can be neurologically dissociated from motivated appetitive behavior. An incentive attribution hypothesis that can account for the results is discussed, along with its implications for a wide range of phenomena associated with dopamine depletion.
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In rats, complete removal of nearly all dopamine by neurochemical brain lesions left sweetness 'liking' completely normal and unimpaired, despite eliminating all 'wanting' to eat.
“Further, even complete removal of nearly all dopamine by neurochemical brain lesions left rats’ sweetness ‘liking’ completely normal and unimpaired, despite eliminating all ‘wanting’ to eat (Berridge et al., 1989).”
From Evolving Concepts of Emotion and Motivation (2018) · cites this paper as Berridge et al., 1989
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“Our data substantiate the delicate role of VTA dopaminergic neurons on explorative locomotion and reward motivation but not reward perception, as also indicated by irreversible lesion studies (Kelly et al., 1975; Roberts and Koob, 1982; Berridge et al., 1989; Berridge and Robinson, 2016).”
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“Similar results have been found after lesions (Berridge et al. 1989; Galaverna et al. 1993; Berridge 1996), electrical stimulation (Berridge and Valenstein 1991) and cooling (Berridge and Zajonc 1991) of dopamine system related structures.”
ResultBakshi, V. P., & Kelley, A. E. (1991) · Psychobiology · doi:10.3758/bf03332072 · Cited by 69 · see citing works
Explanatory pluralism: An unrewarding prediction error for free energy theorists
Colombo, M., & Wright, C. (2017) · Brain and Cognition · doi:10.1016/j.bandc.2016.02.003 · Cited by 67 · see citing works
“In the late 1980s and 1990s, IS was offered to explain the differential effects on ‘liking’ (i.e., subpersonal states of pleasure or hedonic impact) and ‘wanting’ (i.e., incentive salience) of pharmacological manipulations of DA in rats during taste-reactivity tasks (Berridge et al. 1989).”
BackgroundPrefrontal/accumbal catecholamine system processes high motivational salience
Puglisi‐Allegra, S., & Ventura, R. (2012) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2012.00031 · Cited by 70 · see citing works
Schizophrenia in Translation: Dissecting Motivation in Schizophrenia and Rodents
Simpson, E. H., Waltz, J. A., Kellendonk, C., & Balsam, P. D. (2012) · Schizophrenia Bulletin · doi:10.1093/schbul/sbs114 · Cited by 65 · see citing works
Roles of Chemical Mediators in the Taste System
Yamamoto, T., Nagai, T., Shimura, T., & Yasoshima, Y. (1998) · The Japanese Journal of Pharmacology · doi:10.1254/jjp.76.325 · Cited by 64 · see citing works
The Cambridge Handbook of Substance and Behavioral Addictions
Sussman, S. Y. (2020) · Cambridge University Press eBooks · doi:10.1017/9781108632591 · Cited by 63 · see citing works
Camarini, R., & Pautassi, R. M. (2016) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2016.04.006 · Cited by 60 · see citing works
“…in the early 1990s when Robinson and Berridge (1993) proposed the incentive sensitization theory of addiction, which was based on early experimental evidence (Berridge et al., 1989) that indicated a dissociation between motivated, appetitive behavior and the ability to hedonically react to stimuli.”
BackgroundKorb, S., Götzendorfer, S. J., Massaccesi, C., Sezen, P., Graf, I., Willeit, M., Eisenegger, C., & Silani, G. (2020) · eLife · doi:10.7554/elife.55797 · Cited by 51 · see citing works
Lesions of the central nucleus of the amygdala II: Effects on intraoral NaCl intake
Seeley, R. J., Galaverna, O., Schulkin, J. A., Epstein, A. N., & Grill, H. J. (1993) · Behavioural Brain Research · doi:10.1016/0166-4328(93)90147-i · Cited by 61 · see citing works
Schallert, T. J., Petrie, B. F., & Whishaw, I. Q. (1989) · Psychobiology · doi:10.3758/bf03337798 · Cited by 59 · see citing works
The dopamine augmenter L-DOPA does not affect positive mood in healthy human volunteers.
Liggins, J., Pihl, R. O., Benkelfat, C., & Leyton, M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0028370 · Cited by 58 · see citing works
D’Aquila, P. S. (2010) · Neuropharmacology · doi:10.1016/j.neuropharm.2010.01.017 · Cited by 55 · see citing works
Pharmacology of Flavor Preference Conditioning in Sham-Feeding Rats
Yu, W.-Z., Silva, R. M., Sclafani, A. J., Delamater, A. R., & Bodnar, R. J. (2000) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(99)00239-7 · Cited by 58 · see citing works
Hypothalamic Cooling Elicits Eating: Differential Effects on Motivation and Pleasure
Berridge, K. C., & Zajonc, R. B. (1991) · Psychological Science · doi:10.1111/j.1467-9280.1991.tb00128.x · Cited by 56 · see citing works
Self-citationTrait Anticipatory Pleasure Predicts Effort Expenditure for Reward
Geaney, J. T., Treadway, M. T., & Smillie, L. D. (2015) · PLoS ONE · doi:10.1371/journal.pone.0131357 · Cited by 58 · see citing works
“For instance, genetically engineered mice with elevated dopamine availability display hyperactivated approach behavior toward food [10], whereas dopamine-deficient rodents exhibit diminished approach behaviors, but both maintain normal affective taste reactivity to sweet substances [8,11].”
BackgroundReassessing wanting and liking in the study of mesolimbic influence on food intake
Nicola, S. M. (2016) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00234.2016 · Cited by 50 · see citing works
“Strikingly, lesions made with the toxin 6-hydroxydopamine (6-OHDA), which kills VTA and substantia nigra dopamine neurons and reduces dopamine levels in the NAc and neostriatum, cause profound reductions in motor behavior without altering taste hedonics as measured by taste reactivity, strongly arguing that hedonia is…”
BackgroundBerridge, K. C. (1989) · Psychobiology · doi:10.3758/bf03337797 · Cited by 52 · see citing works
Self-citationThe incentive salience of courtship vocalizations: Hormone-mediated ‘wanting’ in the auditory system
Maney, D. L. (2013) · Hearing Research · doi:10.1016/j.heares.2013.04.011 · Cited by 47 · see citing works
Hernández, J. M., Lanuza, E., & Martínez‐Garciá, F. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04944.x · Cited by 50 · see citing works
“The effects of DA lesions (Berridge et al., 1989) and the behaviour of DAT knockdown mutants (Peciña et al.”
BackgroundInfluential
- Authors
- Berridge, K. C., Venier, I. L., & Robinson, T. E.
- Affiliations
- University of Michigan (US)
- Venue
- Behavioral Neuroscience
- Published
- 1989-02
- Volume
- 103
- Issue
- 1
- Pages
- 36-45
- ISSN
- 0735-7044 (ISSN-L)
- 1939-0084
- OpenAlex
- W4239398105
- Cited by
- 356
- References
- 0
- Citations by year
- 2026: 2 · 2025: 14 · 2024: 12 · 2023: 19 · 2022: 12 · 2021: 6 · 2020: 54 · 2019: 42 · 2018: 9 · 2017: 8 · 2016: 10 · 2015: 11 · 2014: 2 · 2013: 7 · 2012: 12
- FWCI
- 2.84
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Behavioral Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (MH-37277)
- National Institute of Neurological Disorders and Stroke (NS-23959)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Keywords
- 6-hydroxydopamine, aphagia, taste reactivity, dopaminergic activity, arousal hypothesis, dopamine depletion, dietary intake
- MeSH terms
- Animals, Feeding and Eating Disorders, Arousal, Dopamine, Hydroxydopamines, Male, Rats, Inbred Strains, Taste, Oxidopamine, Rats
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