Spatiotemporal precision and hemodynamic mechanism of optical point spreads in alert primates
Open accessAbstract
In functional brain imaging there is controversy over which hemodynamic signal best represents neural activity. Intrinsic signal optical imaging (ISOI) suggests that the best signal is the early darkening observed at wavelengths absorbed preferentially by deoxyhemoglobin (HbR). It is assumed that this darkening or "initial dip" reports local conversion of oxyhemoglobin (HbO) to HbR, i.e., oxygen consumption caused by local neural activity, thus giving the most specific measure of such activity. The blood volume signal, by contrast, is believed to be more delayed and less specific. Here, we used multiwavelength ISOI to simultaneously map oxygenation and blood volume [i.e., total hemoglobin (HbT)] in primary visual cortex (V1) of the alert macaque. We found that the hemodynamic "point spread," i.e., impulse response to a minimal visual stimulus, was as rapid and retinotopically specific when imaged by using blood volume as when using the initial dip. Quantitative separation of the imaged signal into HbR, HbO, and HbT showed, moreover, that the initial dip was dominated by a fast local increase in HbT, with no increase in HbR. We found only a delayed HbR decrease that was broader in retinotopic spread than HbO or HbT. Further, we show that the multiphasic time course of typical ISOI signals and the strength of the initial dip may reflect the temporal interplay of monophasic HbO, HbR, and HbT signals. Characterizing the hemodynamic response is important for understanding neurovascular coupling and elucidating the physiological basis of imaging techniques such as fMRI.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
At low field strengths suitable for scanning children and adolescents (<7 T), the PSF in a region of cortex is thought to be largely determined by proximity to local blood vessels, rather than by local grey matter density, horizontal connections, synapses and so on.
“At the low field strengths suitable for scanning children and adolescents (<7 T), the PSF in a region of cortex is thought to be largely determined by proximity to local blood vessels, rather than by local grey matter density, horizontal connections, synapses and so on (Sirotin et al., 2009; Shmuel et al., 2007).”
From The social brain in adolescence: evidence from functional magnetic resonance imaging and behavioural studies (2011) · cites this paper as Sirotin et al., 2009
Cites
Ogawa, S., Tank, D. W., Menon, R., Ellermann, J. M., Kim, S. G., Merkle, H., & Ugurbil, K. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.13.5951 · Cited by 3,681 · see citing works
Functional architecture of cortex revealed by optical imaging of intrinsic signals
Grinvald, A., Lieke, E. E., Frostig, R. D., Gilbert, C. D., & Wiesel, T. N. (1986) · Nature · doi:10.1038/324361a0 · Cited by 1,243 · see citing works
Malonek, D., & Grinvald, A. (1996) · Science · doi:10.1126/science.272.5261.551 · Cited by 1,095 · see citing works
Frostig, R. D., Lieke, E. E., Ts’o, D. Y., & Grinvald, A. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.16.6082 · Cited by 948 · see citing works
Grinvald, A., Lieke, E. E., Rd, F., & Hildesheim, R. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-05-02545.1994 · Cited by 632 · see citing works
Das, A., & Gilbert, C. D. (1995) · Nature · doi:10.1038/375780a0 · Cited by 446 · see citing works
Self-citationAnticipatory haemodynamic signals in sensory cortex not predicted by local neuronal activity
Sirotin, Y. B., & Das, A. (2009) · Nature · doi:10.1038/nature07664 · Cited by 437 · see citing works
Self-citationMenon, R. S., Ogawa, S., Hu, X. P., Strupp, J., Anderson, P., & Uǧurbil, K. (1995) · Magnetic Resonance in Medicine · doi:10.1002/mrm.1910330323 · Cited by 421 · see citing works
High-resolution mapping of iso-orientation columns by fMRI
Kim, D., Duong, T. Q., & Kim, S. (2000) · Nature Neuroscience · doi:10.1038/72109 · Cited by 393 · see citing works
Sheth, S. A., Nemoto, M., Guiou, M., Walker, M., Pouratian, N., & Toga, A. W. (2004) · Neuron · doi:10.1016/s0896-6273(04)00221-1 · Cited by 308 · see citing works
Hillman, E. M. C., Devor, A., Bouchard, M. B., Dunn, A. K., Krauss, G. W., Skoch, J. M., Bacskai, B. J., Dale, A. M., & Boas, D. A. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2006.11.032 · Cited by 290 · see citing works
Self-citationDunn, A. K., Devor, A., Dale, A. M., & Boas, D. A. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.04.024 · Cited by 285 · see citing works
Investigating neural–hemodynamic coupling and the hemodynamic response function in the awake rat
Martin, C. J., Martindale, J., Berwick, J., & Mayhew, J. E. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.02.021 · Cited by 255 · see citing works
Jones, M., Berwick, J., Johnston, D., & Mayhew, J. E. (2001) · NeuroImage · doi:10.1006/nimg.2001.0808 · Cited by 239 · see citing works
Shtoyerman, E., Arieli, A., Slovin, H., Vanzetta, I., & Grinvald, A. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-21-08111.2000 · Cited by 213 · see citing works
Buxton, R. B. (2001) · NeuroImage · doi:10.1006/nimg.2001.0814 · Cited by 211 · see citing works
Vovenko, E. P. (1999) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s004240050825 · Cited by 207 · see citing works
Mapping multiple features in the population response of visual cortex
Basole, A., White, L. E., & Fitzpatrick, D. (2003) · Nature · doi:10.1038/nature01721 · Cited by 191 · see citing works
Optimal decoding of correlated neural population responses in the primate visual cortex
Chen, Y., Geisler, W. S., & Seidemann, E. (2006) · Nature Neuroscience · doi:10.1038/nn1792 · Cited by 191 · see citing works
Water diffusion, T2, and compartmentation in frog sciatic nerve
Peled, S., Cory, D. G., Raymond, S. A., Kirschner, D. A., & Jolesz, F. A. (1999) · Magnetic Resonance in Medicine · doi:10.1002/(sici)1522-2594(199911)42:5 · Cited by 189 · see citing works
Physical model for the spectroscopic analysis of cortical intrinsic optical signals
Kohl‐Bareis, M., Lindauer, U., Royl, G., Kühl, M., Gold, L., Villringer, A., & Dirnagl, U. (2000) · Physics in Medicine and Biology · doi:10.1088/0031-9155/45/12/317 · Cited by 177 · see citing works
Silva, A. C., Lee, P., Iadecola, C., & Kim, S. (2000) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-200001000-00025 · Cited by 165 · see citing works
Lindauer, U., Royl, G., Leithner, C., Kühl, M., Gold, L., Gethmann, J. M., Kohl‐Bareis, M., Villringer, A., & Dirnagl, U. (2001) · NeuroImage · doi:10.1006/nimg.2000.0709 · Cited by 154 · see citing works
Mayhew, J. E., Johnston, D. K., Berwick, J., Jones, M., Coffey, P. J., & Zheng, Y. (2000) · NeuroImage · doi:10.1006/nimg.2000.0656 · Cited by 150 · see citing works
Chisum, H. J., Mooser, F., & Fitzpatrick, D. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-07-02947.2003 · Cited by 132 · see citing works
Berwick, J., Johnston, D., Jones, M., Martindale, J., Martin, C. J., Kennerley, A. J., Redgrave, P., & Mayhew, J. E. W. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00658.2007 · Cited by 131 · see citing works
Compartment-Resolved Imaging of Activity-Dependent Dynamics of Cortical Blood Volume and Oximetry
Vanzetta, I., Hildesheim, R., & Grinvald, A. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.3032-04.2005 · Cited by 119 · see citing works
Nemoto, M., Sheth, S. A., Guiou, M., Pouratian, N., Chen, J. W. Y., & Toga, A. W. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4870-03.2004 · Cited by 108 · see citing works
Moon, C.-H., Fukuda, M., Park, S., & Kim, S.-G. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0445-07.2007 · Cited by 106 · see citing works
The Triphasic Intrinsic Signal: Implications for Functional Imaging
Chen‐Bee, C. H., Agoncillo, T., Xiong, Y., & Frostig, R. D. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0326-07.2007 · Cited by 91 · see citing works
Ances, B. M. (2003) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/01.wcb.0000103920.96801.12 · Cited by 86 · see citing works
Coupling between neuronal activity and microcirculation: Implications for functional brain imaging
Vanzetta, I., & Grinvald, A. (2008) · HFSP journal · doi:10.2976/1.2889618 · Cited by 84 · see citing works
Culver, J. P., Siegel, A. M., Franceschini, M. A., Mandeville, J. B., & Boas, D. A. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.05.052 · Cited by 80 · see citing works
Vanzetta, I., & Grinvald, A. (2001) · NeuroImage · doi:10.1006/nimg.2001.0843 · Cited by 78 · see citing works
Modification of the pharmacokinetics of high-dose cyclophosphamide and cisplatin by antiemetics
Cagnoni, P. J., Matthes, S. G., Day, T., et al. (1999) · Bone Marrow Transplantation · doi:10.1038/sj.bmt.1701832 · Cited by 78 · see citing works
Can current fMRI techniques reveal the micro-architecture of cortex?
Logothetis, N. K. (2000) · Nature Neuroscience · doi:10.1038/74768 · Cited by 74 · see citing works
Dynamics and nonlinearities of the BOLD response at very short stimulus durations
Yesilyurt, B., Uǧurbil, K., & Uludaǧ, K. (2008) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2008.01.008 · Cited by 73 · see citing works
Optical imaging of functional domains in the cortex of the awake and behaving monkey
Vnek, N., Ramsden, B. M., Hung, C. P., Goldman‐Rakic, P. S., & Roe, A. W. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.7.4057 · Cited by 55 · see citing works
Trial-by-trial relationship between neural activity, oxygen consumption, and blood flow responses
Masamoto, K., Vazquez, A. L., Wang, P., & Kim, S. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.12.011 · Cited by 51 · see citing works
Functional Architecture of Eye Position Gain Fields in Visual Association Cortex of Behaving Monkey
Siegel, R. M., Raffi, M., Phinney, R. E., Turner, J. A., & Jandó, G. (2003) · Journal of Neurophysiology · doi:10.1152/jn.01179.2002 · Cited by 43 · see citing works
Intracranial microprobe for evaluating neuro-hemodynamic coupling in unanesthetized human neocortex
Keller, C. J., Cash, S. S., Narayanan, S. N., Wang, C., Kuzniecky, R., Carlson, C., Devinsky, O., Thesen, T., Doyle, W., Sassaroli, A., et al. (2009) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2009.01.036 · Cited by 24 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The cortical angiome: an interconnected vascular network with noncolumnar patterns of blood flow
Blinder, P., Tsai, P. S., Kaufhold, J. P., Knutsen, P. M., Suhl, H., & Kleinfeld, D. (2013) · Nature Neuroscience · doi:10.1038/nn.3426 · Cited by 573 · see citing works
Biophysical and Physiological Origins of Blood Oxygenation Level-Dependent fMRI Signals
Kim, S.-G., & Ogawa, S. (2012) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2012.23 · Cited by 547 · see citing works
Pericyte degeneration leads to neurovascular uncoupling and limits oxygen supply to brain
Kisler, K., Nelson, A. R., Rege, S. V., Ramanathan, A., Wang, Y., Ahuja, A., Lazic, D., Tsai, P. S., Zhao, Z., Zhou, Y., et al. (2017) · Nature Neuroscience · doi:10.1038/nn.4489 · Cited by 497 · see citing works
Burnett, S., Sebastian, C., Cohen Kadosh, K., & Blakemore, S.-J. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.10.011 · Cited by 391 · see citing works
Ma, Y., Shaik, M. A., Kim, S. H., Kozberg, M. G., Thibodeaux, D. N., Zhao, H. T., Yu, H., & Hillman, E. M. C. (2016) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2015.0360 · Cited by 335 · see citing works
Self-citationThe neurovascular unit in brain function and disease: The neurovascular unit function
Lecrux, C., & Hamel, E. (2011) · Acta Physiologica · doi:10.1111/j.1748-1716.2011.02256.x · Cited by 251 · see citing works
Sensory experience modifies feature map relationships in visual cortex
Cloherty, S. L., Hughes, N. J., Hietanen, M. A., Bhagavatula, P. S., Goodhill, G. J., & Ibbotson, M. R. (2016) · eLife · doi:10.7554/elife.13911 · Cited by 24 · see citing works
- Authors
- Sirotin, Y. B., Hillman, E. M. C., Bordier, C., & Das, A.
- Affiliations
- Departments of aNeuroscience,
- Biomedical Engineering,
- New York State Psychiatric Institute (US)
- Corresponding author
- Sirotin, Yevgeniy B.
- Das, Aniruddha
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2009-10-27
- Volume
- 106
- Issue
- 43
- Pages
- 18390-18395
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2775289
- OpenAlex
- W2061951101
- Cited by
- 121
- References
- 41
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 1 · 2023: 6 · 2022: 8 · 2021: 2 · 2020: 3 · 2019: 8 · 2018: 7 · 2017: 9 · 2016: 13 · 2015: 10 · 2014: 8 · 2013: 12 · 2012: 10
- FWCI
- 7.27
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Dana Foundation
- National Institutes of Health (5r24ey015634-05)
- National Institute of Mental Health (T32MH015174)
- National Eye Institute (R24 EY-015634, R01EY019500, R01EY013759)
- National Institute of Neurological Disorders and Stroke (F31NS056834, R21NS053684, R01NS063226)
- Topics
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Optical Imaging and Spectroscopy Techniques
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Keywords
- intrinsic signal imaging, hemodynamic response, deoxyhemoglobin, oxyhemoglobin, total hemoglobin, blood volume, primary visual cortex, macaque, retinotopic mapping, neurovascular coupling, neural activity detection, multi-wavelength imaging
- MeSH terms
- Animals, Hemodynamics, Hemoglobins, Macaca, Magnetic Resonance Imaging, Oximetry, Visual Cortex
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
