IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-46088-z.html
   My bibliography  Save this article

Distinct neurochemical influences on fMRI response polarity in the striatum

Author

Listed:
  • Domenic H. Cerri

    (the University of North Carolina at Chapel Hill
    the University of North Carolina at Chapel Hill
    the University of North Carolina at Chapel Hill)

  • Daniel L. Albaugh

    (the University of North Carolina at Chapel Hill
    the University of North Carolina at Chapel Hill
    the University of North Carolina at Chapel Hill
    Carnegie Mellon University)

  • Lindsay R. Walton

    (the University of North Carolina at Chapel Hill
    the University of North Carolina at Chapel Hill
    the University of North Carolina at Chapel Hill)

  • Brittany Katz

    (the University of North Carolina at Chapel Hill
    the University of North Carolina at Chapel Hill
    the University of North Carolina at Chapel Hill)

  • Tzu-Wen Wang

    (the University of North Carolina at Chapel Hill
    the University of North Carolina at Chapel Hill
    the University of North Carolina at Chapel Hill)

  • Tzu-Hao Harry Chao

    (the University of North Carolina at Chapel Hill
    the University of North Carolina at Chapel Hill
    the University of North Carolina at Chapel Hill)

  • Weiting Zhang

    (the University of North Carolina at Chapel Hill
    the University of North Carolina at Chapel Hill
    the University of North Carolina at Chapel Hill)

  • Randal J. Nonneman

    (the University of North Carolina at Chapel Hill
    the University of North Carolina at Chapel Hill
    the University of North Carolina at Chapel Hill)

  • Jing Jiang

    (Stanford University
    Stanford University
    University of Iowa Carver College of Medicine
    University of Iowa Carver College of Medicine)

  • Sung-Ho Lee

    (the University of North Carolina at Chapel Hill
    the University of North Carolina at Chapel Hill
    the University of North Carolina at Chapel Hill)

  • Amit Etkin

    (Stanford University
    Stanford University
    Alto Neuroscience)

  • Catherine N. Hall

    (University of Sussex
    University of Sussex)

  • Garret D. Stuber

    (University of Washington
    University of Washington
    University of Washington)

  • Yen-Yu Ian Shih

    (the University of North Carolina at Chapel Hill
    the University of North Carolina at Chapel Hill
    the University of North Carolina at Chapel Hill)

Abstract

The striatum, known as the input nucleus of the basal ganglia, is extensively studied for its diverse behavioral roles. However, the relationship between its neuronal and vascular activity, vital for interpreting functional magnetic resonance imaging (fMRI) signals, has not received comprehensive examination within the striatum. Here, we demonstrate that optogenetic stimulation of dorsal striatal neurons or their afferents from various cortical and subcortical regions induces negative striatal fMRI responses in rats, manifesting as vasoconstriction. These responses occur even with heightened striatal neuronal activity, confirmed by electrophysiology and fiber-photometry. In parallel, midbrain dopaminergic neuron optogenetic modulation, coupled with electrochemical measurements, establishes a link between striatal vasodilation and dopamine release. Intriguingly, in vivo intra-striatal pharmacological manipulations during optogenetic stimulation highlight a critical role of opioidergic signaling in generating striatal vasoconstriction. This observation is substantiated by detecting striatal vasoconstriction in brain slices after synthetic opioid application. In humans, manipulations aimed at increasing striatal neuronal activity likewise elicit negative striatal fMRI responses. Our results emphasize the necessity of considering vasoactive neurotransmission alongside neuronal activity when interpreting fMRI signal.

Suggested Citation

  • Domenic H. Cerri & Daniel L. Albaugh & Lindsay R. Walton & Brittany Katz & Tzu-Wen Wang & Tzu-Hao Harry Chao & Weiting Zhang & Randal J. Nonneman & Jing Jiang & Sung-Ho Lee & Amit Etkin & Catherine N., 2024. "Distinct neurochemical influences on fMRI response polarity in the striatum," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46088-z
    DOI: 10.1038/s41467-024-46088-z
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-46088-z
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-46088-z?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Jin Hyung Lee & Remy Durand & Viviana Gradinaru & Feng Zhang & Inbal Goshen & Dae-Shik Kim & Lief E. Fenno & Charu Ramakrishnan & Karl Deisseroth, 2010. "Global and local fMRI signals driven by neurons defined optogenetically by type and wiring," Nature, Nature, vol. 465(7299), pages 788-792, June.
    2. Ravi L Rungta & Bruno-Félix Osmanski & Davide Boido & Mickael Tanter & Serge Charpak, 2017. "Light controls cerebral blood flow in naive animals," Nature Communications, Nature, vol. 8(1), pages 1-9, April.
    3. David Attwell & Alastair M. Buchan & Serge Charpak & Martin Lauritzen & Brian A. MacVicar & Eric A. Newman, 2010. "Glial and neuronal control of brain blood flow," Nature, Nature, vol. 468(7321), pages 232-243, November.
    4. Nikos K. Logothetis & Jon Pauls & Mark Augath & Torsten Trinath & Axel Oeltermann, 2001. "Neurophysiological investigation of the basis of the fMRI signal," Nature, Nature, vol. 412(6843), pages 150-157, July.
    5. Edik M. Blais & Kristopher D. Rawls & Bonnie V. Dougherty & Zhuo I. Li & Glynis L. Kolling & Ping Ye & Anders Wallqvist & Jason A. Papin, 2017. "Reconciled rat and human metabolic networks for comparative toxicogenomics and biomarker predictions," Nature Communications, Nature, vol. 8(1), pages 1-15, April.
    6. Nikos K. Logothetis, 2008. "What we can do and what we cannot do with fMRI," Nature, Nature, vol. 453(7197), pages 869-878, June.
    7. Nan Li & Alan Jasanoff, 2020. "Local and global consequences of reward-evoked striatal dopamine release," Nature, Nature, vol. 580(7802), pages 239-244, April.
    8. Catherine N. Hall & Clare Reynell & Bodil Gesslein & Nicola B. Hamilton & Anusha Mishra & Brad A. Sutherland & Fergus M. O’Farrell & Alastair M. Buchan & Martin Lauritzen & David Attwell, 2014. "Capillary pericytes regulate cerebral blood flow in health and disease," Nature, Nature, vol. 508(7494), pages 55-60, April.
    9. Xuming Chen & Filip Sobczak & Yi Chen & Yuanyuan Jiang & Chunqi Qian & Zuneng Lu & Cenk Ayata & Nikos K. Logothetis & Xin Yu, 2019. "Mapping optogenetically-driven single-vessel fMRI with concurrent neuronal calcium recordings in the rat hippocampus," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Adam Institoris & Milène Vandal & Govind Peringod & Christy Catalano & Cam Ha Tran & Xinzhu Yu & Frank Visser & Cheryl Breiteneder & Leonardo Molina & Baljit S. Khakh & Minh Dang Nguyen & Roger J. Tho, 2022. "Astrocytes amplify neurovascular coupling to sustained activation of neocortex in awake mice," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    2. Rita Gil & Mafalda Valente & Noam Shemesh, 2024. "Rat superior colliculus encodes the transition between static and dynamic vision modes," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    3. Olsen, Carmen & Gold, Anna, 2018. "Future research directions at the intersection between cognitive neuroscience research and auditors’ professional skepticism," Journal of Accounting Literature, Elsevier, vol. 41(C), pages 127-141.
    4. Eva R. Pool & Wolfgang M. Pauli & Logan Cross & John P. O’Doherty, 2023. "Neural substrates of parallel devaluation-sensitive and devaluation-insensitive Pavlovian learning in humans," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    5. Airi Jo-Watanabe & Toshiki Inaba & Takahiro Osada & Ryota Hashimoto & Tomohiro Nishizawa & Toshiaki Okuno & Sayoko Ihara & Kazushige Touhara & Nobutaka Hattori & Masatsugu Oh-Hora & Osamu Nureki & Tak, 2024. "Bicarbonate signalling via G protein-coupled receptor regulates ischaemia-reperfusion injury," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    6. Satoshi Ii & Hiroki Kitade & Shunichi Ishida & Yohsuke Imai & Yoshiyuki Watanabe & Shigeo Wada, 2020. "Multiscale modeling of human cerebrovasculature: A hybrid approach using image-based geometry and a mathematical algorithm," PLOS Computational Biology, Public Library of Science, vol. 16(6), pages 1-28, June.
    7. Doungmo Goufo, Emile F. & Mbehou, Mohamed & Kamga Pene, Morgan M., 2018. "A peculiar application of Atangana–Baleanu fractional derivative in neuroscience: Chaotic burst dynamics," Chaos, Solitons & Fractals, Elsevier, vol. 115(C), pages 170-176.
    8. Irene Neuner & Wolfram Kawohl & Jorge Arrubla & Tracy Warbrick & Konrad Hitz & Christine Wyss & Frank Boers & N Jon Shah, 2014. "Cortical Response Variation with Different Sound Pressure Levels: A Combined Event-Related Potentials and fMRI Study," PLOS ONE, Public Library of Science, vol. 9(10), pages 1-14, October.
    9. Zvi N. Roth & Kendrick Kay & Elisha P. Merriam, 2022. "Natural scene sampling reveals reliable coarse-scale orientation tuning in human V1," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    10. repec:hum:wpaper:sfb649dp2014-036 is not listed on IDEAS
    11. Alejandro Morán & Miguel C Soriano, 2018. "Improving the quality of a collective signal in a consumer EEG headset," PLOS ONE, Public Library of Science, vol. 13(5), pages 1-21, May.
    12. Adam S. Tuzolele Mbuku, 2024. "Evolution of the concept of Homo Economicus in light of advances in Neuroeconomics: towards a more realistic model of economic decision-making [Evolution du concept de l'Homo Economicus à la lumièr," Post-Print hal-04564775, HAL.
    13. Phoebe Koundouri & Barbara Hammer & Ulrike Kuhl & Alina Velias, 2022. "Behavioral and Neuroeconomics of Environmental Values," DEOS Working Papers 2227, Athens University of Economics and Business.
    14. Wan-Yu Shih & Hsiang-Yu Yu & Cheng-Chia Lee & Chien-Chen Chou & Chien Chen & Paul W. Glimcher & Shih-Wei Wu, 2023. "Electrophysiological population dynamics reveal context dependencies during decision making in human frontal cortex," Nature Communications, Nature, vol. 14(1), pages 1-24, December.
    15. Mohammad Haft-Javaherian & Linjing Fang & Victorine Muse & Chris B Schaffer & Nozomi Nishimura & Mert R Sabuncu, 2019. "Deep convolutional neural networks for segmenting 3D in vivo multiphoton images of vasculature in Alzheimer disease mouse models," PLOS ONE, Public Library of Science, vol. 14(3), pages 1-21, March.
    16. Simon A Overduin & Philip Servos, 2008. "Symmetric Sensorimotor Somatotopy," PLOS ONE, Public Library of Science, vol. 3(1), pages 1-6, January.
    17. Amrita Pal & Jennifer A Ogren & Ravi S Aysola & Rajesh Kumar & Luke A Henderson & Ronald M Harper & Paul M Macey, 2021. "Insular functional organization during handgrip in females and males with obstructive sleep apnea," PLOS ONE, Public Library of Science, vol. 16(2), pages 1-22, February.
    18. Gavin Perry & Nathan W Taylor & Philippa C H Bothwell & Colette C Milbourn & Georgina Powell & Krish D Singh, 2020. "The gamma response to colour hue in humans: Evidence from MEG," PLOS ONE, Public Library of Science, vol. 15(12), pages 1-21, December.
    19. Pérez-Centeno, Victor, 2018. "Brain-driven entrepreneurship research: Expanded review and research agenda towards entrepreneurial enhancement," Working Papers 02/18, Institut für Mittelstandsforschung (IfM) Bonn.
    20. Ujwal Chaudhary & Bin Xia & Stefano Silvoni & Leonardo G Cohen & Niels Birbaumer, 2017. "Brain–Computer Interface–Based Communication in the Completely Locked-In State," PLOS Biology, Public Library of Science, vol. 15(1), pages 1-25, January.
    21. Chaogan Yan & Dongqiang Liu & Yong He & Qihong Zou & Chaozhe Zhu & Xinian Zuo & Xiangyu Long & Yufeng Zang, 2009. "Spontaneous Brain Activity in the Default Mode Network Is Sensitive to Different Resting-State Conditions with Limited Cognitive Load," PLOS ONE, Public Library of Science, vol. 4(5), pages 1-11, May.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46088-z. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.