Substance P Weights Striatal Dopamine Transmission Differently within the Striosome-Matrix Axis
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The mammalian striatum has a topographical organization of input-output connectivity, but a complex internal, nonlaminar neuronal architecture comprising projection neurons of two types interspersed among multiple interneuron types and potential local neuromodulators. From this cellular melange arises a biochemical compartmentalization of areas termed striosomes and extrastriosomal matrix. The functions of these compartments are poorly understood but might confer distinct features to striatal signal processing and be discretely governed. Dopamine transmission occurs throughout striosomes and matrix, and is reported to be modulated by the striosomally enriched neuromodulator substance P. However, reported effects are conflicting, ranging from facilitation to inhibition. We addressed whether dopamine transmission is modulated differently in striosome-matrix compartments by substance P.We paired detection of evoked dopamine release at carbon-fiber microelectrodes in mouse striatal slices with subsequent identification of the location of recording sites with respect to μ-opioid receptor-rich striosomes. Substance P had bidirectional effects on dopamine release that varied between recording sites and were prevented by inhibition of neurokinin-1 receptors. The direction of modulation was determined by location within the striosomal-matrix axis: dopamine release was boosted in striosome centers, diminished in striosomal-matrix border regions, and unaffected in the matrix. In turn, this different weighting of dopamine transmission by substance P modified the apparent center-surround contrast of striosomal dopamine signals. These data reveal that dopamine transmission can be differentially modulated within the striosomal-matrix axis, and furthermore, indicate a functionally distinct zone at the striosome-matrix interface, which may have key impacts on striatal integration.
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Inhomogeneous neuronal release of acetylcholine, glutamate and substance P affects dopamine release, which, together with the heterogeneous striosome-matrix compartments, would result in diverse dopamine release.
“Further, inhomogeneous neuronal release of acetylcholine, glutamate and substance P affects dopamine release159–161, which, together with the heterogeneous striosome-matrix compartments, would result in diverse dopamine release.”
From Dopamine reward prediction-error signalling: A two-component response (2016) · cites this paper as [161]
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Muddapu, V. R., Vijayakumar, K., Ramakrishnan, K., & Chakravarthy, V. S. (2020) · arXiv (Cornell University) · doi:10.48550/arxiv.2004.08320 · Cited by 1 · see citing works
Role of the substance P in learning and memory
Favila, N., & Overton, P. G. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-22194-1.00021-5
Axonal regulation of dopamine transmission by striatal neuromodulators
Cragg, S. J., Sulzer, D. L., & Todd, K. (2025) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-443-29867-7.00005-0
Self-citationCoordinated yet asymmetric striatal neuromodulatory dynamics encode associative learningPreprint
Kim, M. J., Yang, Y., Gamage, P. L., Haun, T., Wu, Y., Navarro, D., & Li, N. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.03.17.712528
Coordinated yet asymmetric striatal neuromodulatory dynamics encode associative learningPreprint
Li, N., Kim, M. J., Yang, Y., Gamage, P. L., Haun, T., Wu, Y., & Navarro, D. (2026) · Research Square · doi:10.21203/rs.3.rs-9931881/v1
- Authors
- Brimblecombe, K. R., & Cragg, S. J.
- Affiliations
- University of Oxford (GB)
- Venue
- Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2015-06-17
- Volume
- 35
- Issue
- 24
- Pages
- 9017-9023
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC4469733
- OpenAlex
- W1491902949
- Cited by
- 58
- References
- 53
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 3 · 2023: 5 · 2022: 2 · 2021: 5 · 2020: 6 · 2019: 4 · 2018: 9 · 2017: 6 · 2016: 13
- FWCI
- 3.92
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by
- Locations
- Journal of Neuroscience (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Oxford University Research Archive (ORA) (University of Oxford) (submittedVersion, cc-by)
- Funders
- Parkinson's UK (G-0803, H-1003, G-1103, G-0808)
- Medical Research Council (MR/K013866/1, MR/J004324/1)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- substance P, striosomes, dopamine release, striatum, neurokinin-1 receptor, mu-opioid receptor, striatal projection neurons
- MeSH terms
- Animals, Corpus Striatum, Dopamine, Male, Mice, Inbred C57BL, Synaptic Transmission, Organ Culture Techniques, Substance P, Mice
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