Protracted maturation of forebrain afferent connections of the ventral tegmental area in the rat

Yetnikoff, Leora; Reichard, Rhett A.; Schwartz, Zachary M.; Parsely, Kenneth P.; Zahm, Daniel S.

doi:10.1002/cne.23459

Cited by 30Neurotransmitter Receptor Influence on BehaviorNeural and Behavioral Psychology StudiesNeuroscience and Neuropharmacology Research

Protracted maturation of forebrain afferent connections of the ventral tegmental area in the rat

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Yetnikoff, Leora, Reichard, Rhett A., Schwartz, Zachary M., Parsely, Kenneth P., Zahm, Daniel S.·2014·Journal of Comparative Neurology

DOI 10.1002/cne.23459PMC PMC4217282

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Abstract

The mesocorticolimbic dopamine system has long attracted the interest of researchers concerned with the unique gamut of behavioral and mental health vulnerabilities associated with adolescence. Accordingly, the development of the mesocorticolimbic system has been studied extensively, but almost exclusively with regard to dopaminergic output, particularly in the nucleus accumbens and medial prefrontal cortex. To the contrary, the ontogeny of inputs to the ventral tegmental area (VTA), the source of mesocorticolimbic dopamine, has been neglected. This is not a trivial oversight, as the activity of VTA neurons, which reflects their capacity to transmit information about salient events, is sensitively modulated by inputs. Here, we assessed the development of VTA afferent connections using the β subunit of cholera toxin (Ctβ) as a retrograde axonal tracer in adolescent (postnatal day 39) and early adult (8–9‐week‐old) rats. After intra‐VTA injections of Ctβ, adolescent and early adult animals exhibited qualitatively similar distributions of retrogradely labeled neurons in the sense that VTA‐projecting neurons were present at all of the same rostrocaudal levels in all of the same structures in both age groups. However, quantitation of retrogradely labeled neurons revealed that adolescent brains, compared with early adult brains, had significantly fewer VTA‐projecting neurons preferentially within an interconnected network of cortical and striatopallidal forebrain structures. These findings provide a novel perspective on the development of the mesocorticolimbic dopamine system and may have important implications for age‐dependent specificity in the function of this system, particularly with regard to adolescent impulsivity and mental health vulnerabilities. J. Comp. Neurol. 522:1031–1047, 2014. © 2013 Wiley Periodicals, Inc.

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In rodents, adolescence is increasingly defined as the period from weaning (~PND 21) to neurobiological maturity around two months of age (~PND 60).
“adolescence in rodents is increasingly defined more in line with this larger age window in humans, by counting the period from weaning (~PND 21) where mice and rats gain begin to interact independently with their environments for the first time”
From Adolescent nicotine exposure and persistent neurocircuitry changes: unveiling lifelong psychiatric risks (2025) · cites this paper as [47]
The Materials and Methods (Animals; page unavailable) says rat adolescence is typically conceived as PND 21–55, with early adulthood beginning between PND 55 and 60. That supports the approximate age window, but the passage does not extend the definition to mice or say that PND 21 marks independent interaction with the environment or that PND 60 marks neurobiological maturity. (LLM, conf=0.84)
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Terminals from the Rat Prefrontal Cortex Synapse on Mesoaccumbens VTA Neurons
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Impact of adolescent social experiences on behavior and neural circuits implicated in mental illnesses
Burke, A. R., McCormick, C. M., Pellis, S. M., & Lukkes, J. L. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.01.018 · Cited by 225 · see citing works
Stress in adolescence and drugs of abuse in rodent models: role of dopamine, CRF, and HPA axis
Burke, A. R., & Miczek, K. A. (2014) · Psychopharmacology · doi:10.1007/s00213-013-3369-1 · Cited by 207 · see citing works
Mesocorticolimbic Dopamine Pathways Across Adolescence: Diversity in Development
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dcc orchestrates the development of the prefrontal cortex during adolescence and is altered in psychiatric patients
Manitt, C., Eng, C., Pokinko, M., Ryan, R. T., Torres-Berrío, A., Lopez, J. P., Yogendran, S. V., Daubaras, M. J. J., Grant, A., Schmidt, E. R. E., et al. (2013) · Translational Psychiatry · doi:10.1038/tp.2013.105 · Cited by 125 · see citing works
Sources of input to the rostromedial tegmental nucleus, ventral tegmental area, and lateral habenula compared: A study in rat
Yetnikoff, L., Cheng, A. Y., Lavezzi, H. N., Parsley, K. P., & Zahm, D. S. (2015) · Journal of Comparative Neurology · doi:10.1002/cne.23797 · Cited by 101 · see citing works
Self-citation
Early Adolescence is a Critical Period for the Maturation of Inhibitory Behavior
Reynolds, L. M., Yetnikoff, L., Pokinko, M., Wodzinski, M., Epelbaum, J. G., Lambert, L. C., Cossette, M.-P., Arvanitogiannis, A., & Flores, C. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhy247 · Cited by 75 · see citing works
Self-citation
Adolescent nicotine exposure and persistent neurocircuitry changes: unveiling lifelong psychiatric risks
Reynolds, L. M., Faure, P., & Barik, J. (2025) · Molecular Psychiatry · doi:10.1038/s41380-025-03110-0 · Cited by 26 · see citing works
“Rodents show behavioral and neurobiological markers of development until neurobiological maturity is reached around two months of age (~PND 60) [36, 38, 39, 44 – 47].”
Adolescent dopamine development
Reynolds, L. M., & Flores, C. (2021) · Diagnosis, Management and Modeling of Neurodevelopmental Disorders · doi:10.1016/b978-0-12-817988-8.00026-9 · Cited by 10 · see citing works

Transcriptomic profiling of the ventral tegmental area and nucleus accumbens in rhesus macaques following long-term cocaine self-administration
Vallender, E. J., Goswami, D. B., Shinday, N. M., Westmoreland, S. V., Yao, W., & Rowlett, J. K. (2017) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2017.01.030 · Cited by 31 · see citing works
Infusion of Nicotine in the Ventral Tegmental Area or the Nucleus Accumbens of the Rat Differentially Affects Accumbal Dopamine Release
Nisell, M., Nomikos, G. G., & Svensson, T. H. (1994) · Pharmacology & Toxicology · doi:10.1111/j.1600-0773.1994.tb00373.x · Cited by 201 · see citing works
Self-stimulation of the nucleus accumbens and ventral tegmental area of tsai attenuated by microinjections of spiroperidol into the nucleus accumbens
Mogenson, G. J., Takigawa, M., Robertson, A., & Wu, M. (1979) · Brain Research · doi:10.1016/0006-8993(79)90331-7 · Cited by 117 · see citing works
Cocaine place conditioning strengthens location-specific hippocampal inputs to the nucleus accumbensPreprint
Sjulson, L., Peyrache, A., Cumpelik, A., et al. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/105890 · Cited by 4 · see citing works
Ethanol-Induced Conditioned Place Preference Is Expressed Through a Ventral Tegmental Area Dependent Mechanism.
Bechtholt, A. J., & Cunningham, C. L. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.1.213 · Cited by 124 · see citing works

Authors: Yetnikoff, L., Reichard, R. A., Schwartz, Z. M., Parsely, K. P., & Zahm, D. S.
Affiliations: Saint Louis University (US)
Corresponding author: Yetnikoff, Leora
Zahm, Daniel S.
ORCID: Yetnikoff, Leora
Zahm, Daniel S.
Venue: Journal of Comparative Neurology
Publisher: Wiley
Published: 2014-02-12
Volume: 522
Issue: 5
Pages: 1031-1047
ISSN: 0021-9967 (ISSN-L)
1096-9861
DOI: 10.1002/cne.23459
PMC: PMC4217282
OpenAlex: W1578486795
Cited by: 30
References: 176
Citations by year: 2026: 1 · 2025: 1 · 2024: 2 · 2022: 3 · 2021: 4 · 2019: 1 · 2018: 1 · 2017: 3 · 2016: 5 · 2015: 4 · 2014: 3 · 2013: 2
FWCI: 2.29
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: The Journal of Comparative Neurology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Instituites of Health (NS-23805)
Fonds Québécois de la Recherche sur la Nature et les Technologies
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 › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: ventral tegmental area, mesocorticolimbic dopamine system, afferent connections, forebrain development, adolescent development, early adulthood, retrograde tracing, cortical projections, impulsivity, psychiatric vulnerability
MeSH terms: Afferent Pathways, Age Factors, Animals, Animals, Newborn, Cell Count, Cholera Toxin, Iontophoresis, Male, Neurons, Nucleus Accumbens, Prosencephalon, Rats, Sprague-Dawley, Ventral Tegmental Area, Rats

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Protracted maturation of forebrain afferent connections of the ventral tegmental area in the rat

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