Intrauterine growth restriction increases impulsive behavior and is associated with altered dopamine transmission in both medial prefrontal and orbitofrontal cortex in female rats
Open accessAbstract
Recent studies have implicated a role for impulsivity in the altered eating behaviors and the increased risk for obesity consistently associated with intrauterine growth restriction (IUGR). Changes in dopamine transmission within prefrontal areas are believed to contribute to these adverse outcomes. Here we investigated the impulsive behavior toward a delayed reward and evaluated dopamine levels and its receptors in the medial prefrontal (mPFC) and orbitofrontal (OFC) cortex of female adult rats exposed to IUGR. From day 10 of pregnancy and until birth, Sprague-Dawley dams received either an ad libitum (Adlib) or a 50% food-restricted (FR) diet. At birth, all pups were adopted by Adlib mothers, generating the groups Adlib/Adlib (control) and FR/Adlib (intrauterine growth-restricted). Adult impulsive behavior was evaluated using a Tolerance to Delay of Reward Task. In vivo dopamine responses to sweet food intake were measured by voltammetry, and D1, D2 and DAT levels were accessed by Western Blot. Animals from FR group showed a pronounced aversion to delayed rewards. DA response to sweet food was found to be blunted in the mPFC of FR animals, whereas in the OFC, the DA levels appear to be unaffected by reward consumption. Moreover, FR animals presented reduced D1 receptors in the OFC and a later increase in the mPFC D2 levels. These findings suggest that IUGR female rats are more impulsive and that the associated mechanism involves changes in the dopamine signaling in both the mPFC and OFC.
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IUGR is associated with an increase in impulsive behavior due to an altered dopamine signaling in the PFC.
“Recently it has become clear that IUGR is associated with an increase in impulsive behavior due to an altered dopamine signaling in the PFC [357, 358].”
From Development of prefrontal cortex (2022) · cites this paper as [357]
The Abstract and Discussion report increased impulsive behavior alongside altered dopamine signaling in the prefrontal cortex of female IUGR rats. They describe dopamine changes as an associated, likely mechanism, not a demonstrated cause. The citing sentence states causation more definitively and omits the study's restriction to female rats. (LLM, conf=0.88)
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Mechelmans, D. J., Strelchuk, D., Doñamayor, N., Banca, P., Robbins, T. W., Baek, K., & Voon, V. (2017) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyx072 · Cited by 25 · see citing works
Yates, J. R., Darna, M., Beckmann, J. S., Dwoskin, L. P., & Bardo, M. T. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.11.033 · Cited by 24 · see citing works
Mechanisms of impulsive choice: III. The role of reward processes
Marshall, A. T., & Kirkpatrick, K. (2015) · Behavioural Processes · doi:10.1016/j.beproc.2015.10.013 · Cited by 23 · see citing works
Moscarello, J. M., Ben‐Shahar, O., & Ettenberg, A. (2007) · Brain Research · doi:10.1016/j.brainres.2007.06.064 · Cited by 22 · see citing works
Ledo, A., Lourenço, C. F., Caetano, M., Barbosa, R. M., & Laranjinha, J. A. N. (2014) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-014-0115-0 · Cited by 19 · see citing works
Fernández-Feijóo, C. D., Carrasco, C. C., Villalmazo, N., Romero, J. C., Lorenzo, J. R. F., Jimenez-Chillaron, J., & Camprubí-Camprubí, M. (2017) · PLoS ONE · doi:10.1371/journal.pone.0177468 · Cited by 14 · see citing works
Validation of prospective portion size and latency to eat as measures of reactivity to snack foods
van den Akker, K., Bongers, P., Hanssen, I., & Jansen, A. T. M. (2017) · Appetite · doi:10.1016/j.appet.2017.05.049 · Cited by 9 · see citing works
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Cited by
Sorted by citations
Development of prefrontal cortex
Kolk, S. M., & Rakic, P. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-021-01137-9 · Cited by 378 · see citing works
“Recently it has become clear that IUGR is associated with an increase in impulsive behavior due to an altered dopamine signaling in the PFC [357, 358].”
BackgroundAnderson, G. (2019) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2019.109782 · Cited by 47 · see citing works
Miguel, P. M., Meaney, M. J., & Silveira, P. P. (2023) · Biological Psychiatry · doi:10.1016/j.biopsych.2023.01.008 · Cited by 47 · see citing works
“(33) Reduced intracranial volume and cerebral cortical gray matter (within the first 2 weeks of life)—Tolsa”
Self-citationRaji, H., Dinesh, S., & Sharma, S. (2025) · The Egyptian Journal of Neurology Psychiatry and Neurosurgery · doi:10.1186/s41983-024-00930-9 · Cited by 37 · see citing works
“Dopamine release during the delay-to-reward phase, especially with a conditioned cue present, may encourage selecting larger delayed rewards via its influence on the OFC [6].”
Alberry, B., & Silveira, P. P. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105350 · Cited by 27 · see citing works
“impulsive behavior in females, and is associated with altered dopamine transmission in the PFC and orbitofrontal cortex (Alves et al., 2019).”
Self-citationEarly Influences on Development of Sensory Perception and Eating Habits
Scudine, K. G. D. O., Castelo, P. M., Hoppe, J. P. M., Portella, A. K., & Silveira, P. P. (2024) · Advances in Nutrition · doi:10.1016/j.advnut.2024.100325 · Cited by 20 · see citing works
Self-citationEarly adversity and insulin: neuroendocrine programming beyond glucocorticoids
Batra, A., Latsko, M. S., Portella, A. K., & Silveira, P. P. (2021) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2021.09.003 · Cited by 17 · see citing works
Self-citationBatra, A., Chen, L. M., Wang, Z., Parent, C. I., Pokhvisneva, I., Patel, S. H., Levitan, R. D., Meaney, M. J., & Silveira, P. P. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.704785 · Cited by 16 · see citing works
Self-citationLong-Term Metabolic Consequences of Intrauterine Growth Restriction
Joung, K. E., Lee, J., & Kim, J. H. (2020) · Current Pediatrics Reports · doi:10.1007/s40124-020-00212-x · Cited by 16 · see citing works
Barth, B., Arcego, D. M., Filho, E. J. D. M., de Lima, R. M. S., Parent, C. I., Dalmaz, C., Portella, A. K., Pokhvisneva, I., Meaney, M. J., & Silveira, P. P. (2024) · Scientific Reports · doi:10.1038/s41598-024-78465-5 · Cited by 14 · see citing works
Self-citationMoullé, V. S. F., Frapin, M., Amarger, V., & Parnet, P. (2023) · Nutrients · doi:10.3390/nu15020463 · Cited by 11 · see citing works
“Information regarding maternal adiponectin in the context of IUGR is lacking.”
MethodInfluentialBatra, A., Cuesta, S., Alves, M. B., Restrepo-Lozano, J. M., Giroux, M., Laureano, D. P., Lovato, A. B. M., Miguel, P. M., Machado, T. D., Molle, R. D., et al. (2023) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s204017442300017x · Cited by 10 · see citing works
“22 Our current findings may partially explain the mechanism involved in this relationship.”
BackgroundSelf-citationEarly environmental influences on the orbito-frontal cortex function and its effects on behavior
Ruge, O., Hoppe, J. P. M., Molle, R. D., & Silveira, P. P. (2025) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2025.106013 · Cited by 8 · see citing works
Self-citationEarly adversity and the comorbidity between metabolic disease and psychopathology
Gómez‐Ilescas, A., & Silveira, P. P. (2025) · The Journal of Physiology · doi:10.1113/jp285927 · Cited by 10 · see citing works
“These animals also have changes in attention and impulsivity (Alves et al., 2015; Alves et al., 2019), with a delayed or diminished dopamine release in the NAc and medial prefrontal cortex (mPFC) in response to palatable food presentation measured by chronoamperometry (Alves et al., 2019; Laureano…”
InfluentialSelf-citationGao, S., Chen, J., Xu, Y., Liu, S., Lu, C., Guan, Y., & Yang, X. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2021.06.034 · Cited by 8 · see citing works
Harman, A. R., Contreras-Correa, Z. E., Messman, R. D., Swanson, R. M., & Lemley, C. O. (2022) · Placenta · doi:10.1016/j.placenta.2022.11.008 · Cited by 7 · see citing works
Val‐Laillet, D., Kanzari, A., Guérin, S., Randuineau, G., & Coquery, N. (2020) · Neuroscience Letters · doi:10.1016/j.neulet.2020.135395 · Cited by 7 · see citing works
Alves, J., dos Santos, A. P. B., Vieira, A. D. S., Martini, A. P. R., de Lima, R. M. S., Smaniotto, T. Â., de Moraes, R. O., Gomes, R. F., Acerbi, G. C. D. A., de Assis, E. Z. B., et al. (2024) · Neuroscience · doi:10.1016/j.neuroscience.2024.06.020 · Cited by 4 · see citing works
“B .”
Self-citationMucellini, A. B., Laureano, D. P., Alves, M. B., Molle, R. D., Borges, M. B., Salvador, A. P. D. A., Pokhvisneva, I., Manfro, G. G., & Silveira, P. P. (2024) · Developmental Psychobiology · doi:10.1002/dev.22459 · Cited by 3 · see citing works
Self-citationMiguel, P. M., Barth, B., Batra, A., Alves, M. B., Arcego, D. M., Alberry, B., Molle, R. D., Gómez‐Ilescas, A., Zhang, T., Wen, X., et al. (2026) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2026.106887 · Cited by 2 · see citing works
Self-citationJaramillo-Ospina, A. M., Elgbeili, G., Patel, S. H., Pokhvisneva, I., & Silveira, P. P. (2025) · Communications Biology · doi:10.1038/s42003-025-08750-0 · Cited by 2 · see citing works
“Forexample,inananimalmodelofpoorfetalgrowth that induces increased palatable food intake 50 and impulsivity 51 , insulin completely revertsthealterationsinstriatal dopamine release inresponse to T a b l e 4 | M od e r a t o r e ff ec t o f e P R S -”
Self-citationBischoff, A. R., Molle, R. D., Mucellini, A. B., Pokhvisneva, I., Levitan, R. D., Meaney, M. J., & Silveira, P. P. (2023) · Stress · doi:10.1080/10253890.2023.2294954 · Cited by 1 · see citing works
“” “Wanting” is dependent on mesolimbic dopamine circuits and related to the motivation to acquire the reward, whereas ‘‘liking” is related to the elicited pleasure per se and has the opioid system as the main circuit involved (Berridge, 2009a). in the present study, we observed that the altered “liking” behavior of FR…”
InfluentialSelf-citationIntrauterine growth restriction and sugar consumption at two years of age in the BRISA cohort
Aristizábal, L. Y. G., Confortin, S. C., Carneiro, J. R., Ribeiro, C. C. C., Batista, R. F. L., Alves, M. T. S. S. D. B. E., Simões, V. M. F., & da Sílva, A. A. M. (2025) · BMC Pediatrics · doi:10.1186/s12887-025-05448-4 · Cited by 1 · see citing works
Self-citationAlberry, B., Barth, B., Batra, A., Alves, M. B., Miguel, P. M., O’Toole, N., Patel, S., Lupinsky, D., Zhang, T., Wen, X., et al. (2026) · Molecular Metabolism · doi:10.1016/j.molmet.2026.102405 · Cited by 1 · see citing works
“Similar to humans born SGA, FR rodents show an increased preference for sweet rewards [34], have altered hedonic taste reactivity to sweet foods [35], and increased palatable food intake [36].”
Self-citationNeurodegenerative and metabolic disorders, mediated by the trace amines and their receptors
Apryatin, S. A., Karpenko, M. N., Muruzheva, Z. M., Bolshakova, M. V., Magazenkova, D. N., & Клименко, В. М. (2020) · Medical academic journal · doi:10.17816/maj25746 · Cited by 1 · see citing works
“Список сокращений БП — болезнь Паркинсона; мРНК — матричная рибонуклеиновая кислота; НРН — негативная реакция несоответствия; ОВР — ограничение внутриутробного развития; ОП — ограничение питания; СА — следовые амины; ФЭА — β-фенилэтиламин; цАМФ — циклический аденозинмонофосфат; AKT/GSK3 — протеинкиназа B/киназа 3 глик…”
InfluentialAssociation of increased abdominal adiposity at birth with altered ventral caudate microstructure
Koh, D. X. P., Tint, M. T., Gluckman, P. D., Chong, Y. S., Yap, F. K. P., Qiu, A., Eriksson, J. G., Fortier, M. V., Silveira, P. P., Meaney, M. J., et al. (2021) · International Journal of Obesity · doi:10.1038/s41366-021-00905-3 · Cited by 1 · see citing works
“Studies in animal models of poor fetal growth have shown that alterations in dopamine neurotransmission in mesocorticolimbic areas are associated with impulsive eating [62] and increased intake of palatable foods [63], responses that are modulated by peripheral insulin availability [63].”
BackgroundSelf-citationUberos, J., Carrasco-Solís, M. E., Láynez-Rubio, C., Nieto-Ruíz, A., Ruiz‐López, A., Contreras‐Chova, F., Fernández‐Marin, E., Molina-Oya, M., & Campos‐Martínez, A. (2025) · Pediatrics & Neonatology · doi:10.1016/j.pedneo.2025.08.012
Hoppe, J. P. M., Ruge, O., Molle, R. D., Elgbeili, G., Xia, Q., & Silveira, P. P. (2026) · Communications Biology · doi:10.1038/s42003-026-10983-6
Self-citationBenetti, C. D. S., Portella, A. K., Vido, H. G., Fontella, F. U., Noschang, C., Dalmaz, C., Goldani, M. Z., & Silveira, P. P. (2026) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174426100828
Self-citationHarvison, M., & Silveira, P. P. (2026) · Handbook of clinical neurology · doi:10.1016/b978-0-443-19043-8.00004-9
Self-citation
- Authors
- Alves, M. B., Laureano, D. P., Dalle Molle, R., Machado, T. D., Salvador, A. P. D. A., Miguel, P. M., Lupinsky, D., Dalmaz, C., & Silveira, P. P.
- Affiliations
- Universidade Federal do Rio Grande do Sul (BR)
- Douglas Mental Health University Institute (CA)
- Corresponding author
- Alves, Márcio Bonesso
- ORCID
- Venue
- Physiology & Behavior
- Publisher
- Elsevier BV
- Published
- 2019-05
- Volume
- 204
- Pages
- 336-346
- ISSN
- 0031-9384 (ISSN-L)
- OpenAlex
- W2921421048
- Cited by
- 30
- References
- 104
- Citations by year
- 2026: 5 · 2025: 6 · 2024: 4 · 2023: 5 · 2022: 1 · 2021: 5 · 2020: 3 · 2019: 1
- FWCI
- 1.20
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Physiology & Behavior (publishedVersion)
- PubMed (publishedVersion)
- Lume (Universidade Federal do Rio Grande do Sul) (submittedVersion, cc-by-nc-sa)
- Funders
- Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
- Keywords
- fetal growth restriction, impulsivity, delayed rewards, dopamine signaling, medial prefrontal cortex, orbitofrontal cortex, dopamine D1 receptor, dopamine D2 receptor, dopamine transporter, maternal food restriction, female rats, dietary habits, obesity risk
- MeSH terms
- Animals, Behavior, Animal, Dopamine, Female, Fetal Growth Retardation, Impulsive Behavior, Synaptic Transmission, Pregnancy, Prenatal Exposure Delayed Effects, Rats, Sprague-Dawley, Prefrontal Cortex, Rats
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