Microstimulation of primate neocortex targeting striosomes induces negative decision‐making
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Abstract
Here, we combined MRI ‐guided electrical microstimulation and viral tracing to examine the function of a corticostriatal circuit implicated by previous cortical microstimulation as modulating affective judgment and decision‐making. Local microstimulation of a small part of the pregenual anterior cingulate cortex ( pACC ) was found to increase avoidance decisions in a cost‐benefit decision‐making task (Ap‐Av task) in which differing amounts of “good” and “bad” options were given simultaneously. No effect of such stimulation was found when the monkeys performed a task in which both offers were rewarding, but given in different amounts. We asked whether we could identify the targets of such corticostriatal circuits when the cortical microstimulation sites were explicitly identified as affecting approach or avoidance in the Ap‐Av task. We explored the pACC and caudal orbitofrontal cortex ( cOFC ) to look for such sites. For each cortical region, we found sites at which microstimulation induced increased avoidance behavior. After identifying these sites, we injected viral tracers carrying constructs allowing subsequent track‐tracing post‐mortem. For each site identified behaviorally as increasing avoidance choices, we found strong fiber projections to the anterior striatum with large parts of these targeting striosomes subsequently identified by serial section immunohistochemistry. With fMRI , we demonstrated that microstimulation in an anesthetized monkey at sites pre‐identified as affecting Ap‐Av choices induced blood oxygen level dependent activation of the anterior striatum, confirming that the microstimulation method that we applied was effective in activating the striatum. These findings outline circuits leading from pACC / cOFC to striosomes and causally modulating decision‐making under emotional conflict.
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Stimulation of the striosomes of the striatum to which the pgACC region projects induces a negative bias.
“stimulation of the striosomes of the striatum to which this region projects also induces a negative bias [202]”
From Prefrontal cortex and depression (2022) · cites this paper as [202]
The Results report that microstimulation of pACC sites increased avoidance choices and that those sites preferentially projected to striosomes. The paper stimulated the cortex, not the striosomes directly, so it does not establish that stimulation of striosomes induces the negative bias. (LLM, conf=0.87)
Experimental — accuracy not yet measuredMicrostimulation of the caudal OFC in macaques induces a negative bias.
“Akin to microstimulation in pgACC, microstimulation of the caudal OFC in macaques also induces a negative bias [202].”
From Prefrontal cortex and depression (2022) · cites this paper as [202]
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Cites
Neurotransmitters and neuromodulators in the basal ganglia
Graybiel, A. M. (1990) · Trends in Neurosciences · doi:10.1016/0166-2236(90)90104-i · Cited by 1,576 · see citing works
Self-citationSchmahmann, J. D., & Pandya, D. N. (2006) · doi:10.1093/acprof:oso/9780195104233.001.0001 · Cited by 1,157 · see citing works
The Rhesus Monkey Brain in Stereotaxic Coordinates
Paxinos, G., Huang, X., & Toga, A. W. (1999) · Research Online (University of Wollongong) · Cited by 1,070 · see citing works
Frontocingulate Dysfunction in Depression: Toward Biomarkers of Treatment Response
Pizzagalli, D. A. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.166 · Cited by 945 · see citing works
Ghashghaei, H. T., Hilgetag, C. C., & Barbas, H. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2006.09.046 · Cited by 845 · see citing works
Graybiel, A. M., & Ragsdale, C. W. (1978) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.75.11.5723 · Cited by 784 · see citing works
Self-citationForward frontal fields: phylogeny and fundamental function
Wise, S. P. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2008.08.008 · Cited by 478 · cited 1× · see citing works
“Examining these cortico‐striosomal circuits in non‐human primates, therefore, has special value (Wise, 2008), as their decision‐related circuitry is considered to be more nearly homologous to cortical regions that in humans (Neubert, Mars, Sallet, & Rushworth, 2015) are implicated in neuropsychiatric disorders (Pizzag…”
BackgroundPatches with Links: A Unified System for Processing Faces in the Macaque Temporal Lobe
Moeller, S., Freiwald, W. A., & Tsao, D. Y. (2008) · Science · doi:10.1126/science.1157436 · Cited by 402 · see citing works
Highly restricted origin of prefrontal cortical inputs to striosomes in the macaque monkey
Eblen, F., & Graybiel, A. M. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-09-05999.1995 · Cited by 391 · see citing works
Self-citationNeubert, F.-X., Mars, R. B., Sallet, J., & Rushworth, M. F. S. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1410767112 · Cited by 365 · see citing works
Bottom-Up Dependent Gating of Frontal Signals in Early Visual Cortex
Ekstrom, L. B., Roelfsema, P. R., Arsenault, J. T., Bonmassar, G., & Vanduffel, W. (2008) · Science · doi:10.1126/science.1153276 · Cited by 329 · see citing works
Circuit-Based Corticostriatal Homologies Between Rat and Primate
Heilbronner, S. R., Rodríguez-Romaguera, J., Quirk, G. J., Groenewegen, H. J., & Haber, S. N. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.05.012 · Cited by 321 · see citing works
A Corticostriatal Path Targeting Striosomes Controls Decision-Making under Conflict
Friedman, A., Homma, D., Gibb, L. G., Amemori, K.-I., Rubin, S. J., Hood, A. S., Riad, M. H., & Graybiel, A. M. (2015) · Cell · doi:10.1016/j.cell.2015.04.049 · Cited by 309 · see citing works
Self-citationRepeated fMRI Using Iron Oxide Contrast Agent in Awake, Behaving Macaques at 3 Tesla
Leite, F., Tsao, D. Y., Vanduffel, W., Fize, D., Sasaki, Y., Wald, L. L., Dale, A. M., Kwong, K. K., Orban, G. A., Rosen, B. R., et al. (2002) · NeuroImage · doi:10.1006/nimg.2002.1110 · Cited by 269 · see citing works
Fujiyama, F., Sohn, J., Nakano, T., Furuta, T., Nakamura, K., Matsuda, W., & Kaneko, T. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07564.x · Cited by 266 · see citing works
Localized microstimulation of primate pregenual cingulate cortex induces negative decision-making
Amemori, K.-I., & Graybiel, A. M. (2012) · Nature Neuroscience · doi:10.1038/nn.3088 · Cited by 262 · see citing works
Self-citationMapping Cortical Activity Elicited with Electrical Microstimulation Using fMRI in the Macaque
Tolias, A. S., Sultan, F. R., Augath, M. A., Oeltermann, A., Tehovnik, E. J., Schiller, P. H., & Logothetis, N. K. (2005) · Neuron · doi:10.1016/j.neuron.2005.11.034 · Cited by 250 · see citing works
Multiple signals in anterior cingulate cortex
Kolling, N., Behrens, T., Wittmann, M., & Rushworth, M. (2016) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2015.12.007 · Cited by 249 · see citing works
Brimblecombe, K. R., & Cragg, S. J. (2016) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.6b00333 · Cited by 201 · see citing works
Functional anatomy of the basal ganglia in X‐linked recessive dystonia‐parkinsonism
Goto, S., Lee, L. V., Muñoz, E. L., Tooyama, I., Tamiya, G., Makino, S., Ando, S., Dantes, M. B., Yamada, K., Matsumoto, S., et al. (2005) · Annals of Neurology · doi:10.1002/ana.20513 · Cited by 191 · see citing works
Self-citationStriosomes and mood dysfunction in Huntington's disease
Tippett, L. J., Waldvogel, H. J., Thomas, S. J., Hogg, V. M., van Roon‐Mom, W., Synek, B. J. L., Graybiel, A. M., & Faull, R. L. M. (2006) · Brain · doi:10.1093/brain/awl243 · Cited by 165 · see citing works
Self-citationChronic Stress Alters Striosome-Circuit Dynamics, Leading to Aberrant Decision-Making
Friedman, A., Homma, D., Bloem, B., Gibb, L. G., Amemori, K.-I., Hu, D., Delcasso, S., Truong, T. F., Yang, J., Hood, A. S., et al. (2017) · Cell · doi:10.1016/j.cell.2017.10.017 · Cited by 162 · see citing works
Self-citationEnkephalin Disinhibits Mu Opioid Receptor-Rich Striatal Patches via Delta Opioid Receptors
Banghart, M. R., Neufeld, S. Q., Wong, N. C., & Sabatini, B. L. (2015) · Neuron · doi:10.1016/j.neuron.2015.11.010 · Cited by 94 · see citing works
Matsui, T., Tamura, K., Koyano, K. W., Takeuchi, D., Adachi, Y., Osada, T., & Miyashita, Y. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr019 · Cited by 82 · see citing works
Amemori, K., Amemori, S., Gibson, D. J., & Graybiel, A. M. (2018) · Neuron · doi:10.1016/j.neuron.2018.07.022 · Cited by 65 · see citing works
Self-citationReward-Predictive Neural Activities in Striatal Striosome Compartments
Yoshizawa, T., Ito, M., & Doya, K. (2018) · eNeuro · doi:10.1523/eneuro.0367-17.2018 · Cited by 53 · see citing works
Amemori, K.-I., Amemori, S., & Graybiel, A. M. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.1731-14.2015 · Cited by 49 · see citing works
Self-citationPredominant Striatal Input to the Lateral Habenula in Macaques Comes from Striosomes
Hong, S., Amemori, S., Chung, E., Gibson, D. J., Amemori, K., & Graybiel, A. M. (2018) · Current Biology · doi:10.1016/j.cub.2018.11.008 · Cited by 43 · see citing works
Self-citationSaga, Y., Ruff, C. C., & Tremblay, L. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.14201 · Cited by 35 · see citing works
A non-invasive head-holding device for chronic neural recordings in awake behaving monkeys
Amemori, S., Amemori, K., Cantor, M. L., et al. (2014) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2014.11.006 · Cited by 19 · see citing works
Self-citationEvidence for Cholinergic Dysfunction in Autosomal Dominant Kufs Disease
Jarrett, P. G., Easton, A. S., Rockwood, K. J., Dyack, S., McCollum, A., Siu, V. M., Mirsattari, S. M., Massot‐Tarrús, A., Beis, M. J., D’Souza, N., et al. (2017) · Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques · doi:10.1017/cjn.2017.261 · Cited by 10 · see citing works
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Prefrontal cortex and depression
Pizzagalli, D. A., & Roberts, A. C. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-021-01101-7 · Cited by 644 · see citing works
- Authors
- Amemori, S., Amemori, K., Yoshida, T., Papageorgiou, G. K., Xu, R., Shimazu, H., Desimone, R., & Graybiel, A. M.
- Affiliations
- McGovern Institute for Brain Research (US)
- Corresponding author
- Graybiel, Ann M.
- ORCID
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2019-09-23
- Volume
- 51
- Issue
- 3
- Pages
- 731-741
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- PMC
- PMC7031011
- OpenAlex
- W2969994900
- Cited by
- 31
- References
- 31
- Citations by year
- 2026: 8 · 2025: 2 · 2024: 6 · 2023: 2 · 2022: 3 · 2021: 7 · 2020: 3
- FWCI
- 1.89
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Licence
- Locations
- European Journal of Neuroscience (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-sa)
- Funders
- National Institute of Neurological Disorders and Stroke (R01 NS025529)
- Ministry of Education, Culture, Sports, Science and Technology (18H04943, 18H05131)
- Uehara Memorial Foundation
- Office of Naval Research (N00014‐07‐1‐0903)
- Naito Foundation
- CHDI Foundation (A‐5552)
- Army Research Office (W911NF‐16‐1‐0474)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- corticostriatal circuits, striosomes, pregenual anterior cingulate cortex, cost-benefit decision making, emotional conflict, affective judgment, viral tracing, monkeys
- MeSH terms
- Animals, Basal Ganglia, Corpus Striatum, Electric Stimulation, Gyrus Cinguli, Primates, Neocortex
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