The DOI matches its Crossref record; 69 of the 69 references it cites were found in a registry or an index.
Differential Innervation of Direct- and Indirect-Pathway Striatal Projection Neurons
Open accessAbstract
The striatum integrates information from multiple brain regions to shape motor learning. The two major projection cell types in striatum target different downstream basal ganglia targets and have opposing effects on motivated behavior, yet differential innervation of these neuronal subtypes is not well understood. To examine whether input specificity provides a substrate for information segregation in these circuits, we used a monosynaptic rabies virus system to generate brain-wide maps of neurons that form synapses with direct- or indirect-pathway striatal projection neurons. We discovered that sensory cortical and limbic structures preferentially innervated the direct pathway, whereas motor cortex preferentially targeted the indirect pathway. Thalamostriatal input, dopaminergic input, as well as input from specific cortical layers, was similar onto both pathways. We also confirm synaptic innervation of striatal projection neurons by the raphe and pedunculopontine nuclei. Together, these findings provide a framework for guiding future studies of basal ganglia circuit function.
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“we failed to observe vasopressinergic input to CA2 from the paraventricular nucleus of the hypothalamus13, which may reflect an inability of the transsynaptic rabies tracing system to label peptidergic inputs15.”
From The hippocampal CA2 region is essential for social memory (2014) · cites this paper as [15]
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“It sends a direct, likely inhibitory33, projection to the striatum30,34,35 and is, thus, poised to oppose striatal activity.”
From A dual-pathway architecture for stress to disrupt agency and promote habit (2025) · cites this paper as [34]
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“rabies-labeled, DMS D1-projecting cell bodies in the BLA and CeA (right), consistent with prior reports30,34.”
From A dual-pathway architecture for stress to disrupt agency and promote habit (2025) · cites this paper as [34]
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Cites
The functional anatomy of basal ganglia disorders
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Wickersham, I. R., Sullivan, H., & Seung, H. (2010) · Nature Protocols · doi:10.1038/nprot.2009.248 · Cited by 4,905
Primate models of movement disorders of basal ganglia origin
DeLong, M. R. (1990) · Trends in Neurosciences · doi:10.1016/0166-2236(90)90110-v · Cited by 3,824
D 1 and D 2 Dopamine Receptor-regulated Gene Expression of Striatonigral and Striatopallidal Neurons
Gerfen, C. R., Engber, T. M., Mahan, L. C., Susel, Z., Chase, T. N., Monsma, F. J., & Sibley, D. R. (1990) · Science · doi:10.1126/science.2147780 · Cited by 2,967
THE BASAL GANGLIA: FOCUSED SELECTION AND INHIBITION OF COMPETING MOTOR PROGRAMS
Mink, J. W. (1996) · Progress in Neurobiology · doi:10.1016/s0301-0082(96)00042-1 · Cited by 2,478
Dopamine in motivational control: rewarding, aversive, and alerting
Bromberg-Martin, E. S., Matsumoto, M., & Hikosaka, O. (2010) · Neuron · doi:10.1016/j.neuron.2010.11.022 · Cited by 2,396
By Carrot or by Stick: Cognitive Reinforcement Learning in Parkinsonism
Frank, M. J., Seeberger, L. C., & O'Reilly, R. C. (2004) · Science · doi:10.1126/science.1102941 · Cited by 1,964
Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry
Kravitz, A. V., Freeze, B. S., Parker, P. R. L., Kay, K., Thwin, M. T., Deisseroth, K., & Kreitzer, A. C. (2010) · Nature · doi:10.1038/nature09159 · Cited by 1,885
Self-citationThe organization of the projection from the cerebral cortex to the striatum in the rat
McGeorge, A. J., & Faull, R. L. M. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90128-0 · Cited by 1,360
Role of the Basal Ganglia in the Control of Purposive Saccadic Eye Movements
Hikosaka, O., Takikawa, Y., & Kawagoe, R. (2000) · Physiological Reviews · doi:10.1152/physrev.2000.80.3.953 · Cited by 1,334
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Research works printed but not linked: 1
- Smith, 1998, Microcircuitry of the direct and indirect pathways of the basal ganglia, Neuroscience, 86, 353
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The hippocampal CA2 region is essential for social memory
Hitti, F. L., & Siegelbaum, S. A. (2014) · Nature · doi:10.1038/nature13028 · Cited by 976
Striatal circuits for reward learning and decision-making
Cox, J., & Witten, I. B. (2019) · Nature reviews. Neuroscience · doi:10.1038/s41583-019-0189-2 · Cited by 584
A comprehensive excitatory input map of the striatum reveals novel functional organization
Hunnicutt, B. J., Jongbloets, B. C., Birdsong, W. T., Gertz, K. J., Zhong, H., & Mao, T. (2016) · eLife · doi:10.7554/elife.19103 · Cited by 536
A whole-brain atlas of inputs to serotonergic neurons of the dorsal and median raphe nuclei
Pollak Dorocic, I., Fürth, D., Xuan, Y., Johansson, Y., Pozzi, L., Silberberg, G., Carlén, M., & Meletis, K. (2014) · Neuron · doi:10.1016/j.neuron.2014.07.002 · Cited by 451
Pathophysiology of L-dopa-induced motor and non-motor complications in Parkinson's disease
Bastide, M. F., Meissner, W. G., Picconi, B., Fasano, S., Fernagut, P., Feyder, M. T., Francardo, V., Alcacer, C., Ding, Y., Brambilla, R., et al. (2015) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.07.002 · Cited by 492
Metadata
- Authors
- Wall, N. R., De La Parra, M., Callaway, E. M., & Kreitzer, A. C.
- Affiliations
- Salk Institute for Biological Studies (US)
- Gladstone Institutes (US)
- Corresponding author
- Callaway, Edward M.
- Kreitzer, Anatol C.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2013-07
- Volume
- 79
- Issue
- 2
- Pages
- 347-360
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC3729794
- OpenAlex
- W2074651284
- Cited by
- 489
- References
- 69
- Citations by year
- 2026: 19 · 2025: 33 · 2024: 39 · 2023: 40 · 2022: 28 · 2021: 44 · 2020: 38 · 2019: 36 · 2018: 42 · 2017: 48 · 2016: 53 · 2015: 34 · 2014: 32 · 2013: 3
- FWCI
- 25.83
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Gatsby Charitable Foundation
- National Institutes of Health
- National Institute of Mental Health (MH063912, R01MH063912)
- National Institute on Drug Abuse (P01DA010154, DA-010154)
- National Institute of Neurological Disorders and Stroke (NS064984, R01NS078435, R01NS064984)
- Topics
- Health Sciences › Medicine › Clinical Neurology › Deep Brain Stimulation and Movement Disorders
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- striatum, direct pathway, indirect pathway, striatal projection neurons, synaptic innervation, basal ganglia, dopaminergic input, motor cortex, sensory cortex, limbic structures, raphe nuclei, information segregation, motor learning
- MeSH terms
- Animals, Cerebral Cortex, Corpus Striatum, Female, Humans, Male, Mice, Inbred C57BL, Mice, Transgenic, Nerve Net, Neural Pathways, Neurons, Mice, HEK293 Cells
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