Mapping human visual cortex with positron emission tomography
Abstract
Positron-emission tomography (PET) can localize functions of the human brain by imaging regional cerebral blood flow (CBF) during voluntary behaviour. Functional brain mapping with PET, however, has been hindered by PET's poor spatial resolution (typically greater than 1 cm). We have developed an image-analysis strategy that can map functional zones not resolved by conventional PET images. Brain areas selectively activated by a behavioural task can be isolated by subtracting a paired control-state image from the task-state image, thereby removing areas not recruited by the task. When imaged in isolation the centre of an activated area can be located very precisely. This allows subtle shifts in response locale due to changes in task to be detected readily despite poor spatial resolution. As an initial application of this strategy we mapped the retinal projection topography of human primary visual cortex. Functional zones separated by less than 3 mm (centre-to-centre) were differentiated using PET CBF images with a spatial resolution of 18 mm. This technique is not limited to a particular brain area or type of behaviour but does require that the increase in CBF produced by the task be both intense and focal.
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Peak activations in V1 and secondary visual areas are stimulation dependent and occur at distinct temporal frequencies (4 or 8 Hz in V1, and 20 or 40 Hz in secondary visual areas for chromatic or luminance flickering, respectively).
“Previous literature reported that the peak activations in V1 and secondary visual areas are stimulation dependent and occur at distinct temporal frequencies (4 or 8 Hz in V1, and 20 or 40 Hz in secondary visual areas for chromatic or luminance flickering, respectively) (Chai et al., 2019; Fox et al., 1986; Kastner et al., 2004; Kwong et al., 1992; Singh et al., 2000).”
From Perception is associated with the brain’s metabolic response to sensory stimulation (2022) · cites this paper as Fox et al., 1986
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ResultInfluentialEggebrecht, A. T., White, B. R., Ferradal, S. L., Chen, C., Zhan, Y., Snyder, A. Z., Dehghani, H., & Culver, J. P. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.01.124 · Cited by 240 · see citing works
“Visual activations were used because they have served extensively as a substrate for validation by other neuroimaging methodologies (Belliveau et al., 1991; Engel et al., 1997; Fox et al., 1986; Fox et al., 1985) and because the structure and function of the visual cortex has been comprehensively mapped via invasive a…”
Mintun, M. A., Fox, P. T., & Raichle, M. E. (1989) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1989.13 · Cited by 240 · see citing works
Noninvasive Functional Imaging of Human Brain Using Light
Benaron, D. A., Hintz, S. R., Villringer, A., Boas, D. A., Kleinschmidt, A. K., Frahm, J., Hirth, C., Obrig, H., van Houten, J. P., Kermit, E. L., et al. (2000) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-200003000-00005 · Cited by 238 · see citing works
Mixed blocked/event-related designs separate transient and sustained activity in fMRI
Visscher, K. M., Miezin, F. M., Kelly, J. E., Buckner, R., Donaldson, D., McAvoy, M. P., Bhalodia, V. M., & Petersen, S. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00178-2 · Cited by 273 · see citing works
“Similar stimuli have been shown to elicit robust and well-localized hemodynamic responses (Fox et al., 1986; Boynton et al., 1996; Menon and Goodyear , 1999; Miezin et al., 2000; Ollinger et al., 2001b).”
BackgroundVisually evoked activity in cortical cells imaged in freely moving animals
Sawinski, J., Wallace, D. J., Greenberg, D. S., Grossmann, S., Denk, W. T., & Kerr, J. N. D. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0903680106 · Cited by 233 · see citing works
Frequency-Dependent Changes of Regional Cerebral Blood Flow during Finger Movements
Sadato, N., Ibañez, V., Deiber, M., Campbell, G., Leonardo, M., & Hallett, M. (1996) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-199601000-00003 · Cited by 230 · see citing works
The cognitive neuroscience revolution
Boone, W., & Piccinini, G. (2015) · Synthese · doi:10.1007/s11229-015-0783-4 · Cited by 223 · see citing works
In-vivo Optical Imaging of Cortical Architecture and Dynamics
Grinvald, A., Shoham, D., Shmuel, A., Glaser, D. E., Vanzetta, I., Shtoyerman, E., Slovin, H., Wijnbergen, C., Hildesheim, R., & Arieli, A. (1999) · Springer eBooks · doi:10.1007/978-3-642-58552-4_34 · Cited by 222 · see citing works
“Modern imaging techniques have indeed demonstrated that there is a strong coupling between neuronal activity, local metabolic activity, and blood flow (Kety et al., 1955; Lassen and Ingvar, 1961; Sokoloff, 1977; Raichle et al., 1983; Fox et al., 1986).”
Cannon, D. M., Ichise, M., Rollis, D., Klaver, J. M., Gandhi, S. K., Charney, D. S., Manji, H. K., & Drevets, W. C. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.03.016 · Cited by 219 · see citing works
Identifying objects seen from different viewpoints A PET investigation
Kosslyn, S. M., Alpert, N. M., Thompson, W. L., Chabris, C. F., Rauch, S. L., & Anderson, A. K. (1994) · Brain · doi:10.1093/brain/117.5.1055 · Cited by 215 · see citing works
“Holmes, 1918) and PET studies (Fox et al., 1986). Moreover, Kosslyn et al. (1993) used PET to show that topographically organized regions of visual cortex could be activated by visual mental imagery.”
Spatial and temporal limits in cognitive neuroimaging with fMRI
Menon, R. S., & Kim, S.-G. (1999) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(99)01329-7 · Cited by 209 · see citing works
Brain Imaging: Applications in Psychiatry
Andreasen, N. C. (1988) · Science · doi:10.1126/science.3279509 · Cited by 209 · see citing works
Functional and cortical adaptations to central vision loss
Cheung, S. H., & Legge, G. E. (2005) · Visual Neuroscience · doi:10.1017/s0952523805222071 · Cited by 206 · see citing works
“~Fox et al., 1984!. Change in blood flow is marked by the preinjected radioactive water and can be imaged by a PET scanner.”
BackgroundMethodPersistence of abnormal neural responses to a meal in postobese individuals
DelParigi, A., Chen, K., Salbe, A. D., Hill, J. O., Wing, R. R., Reiman, E. M., & Tataranni, P. A. (2003) · International Journal of Obesity · doi:10.1038/sj.ijo.0802558 · Cited by 189 · see citing works
Three-Dimensional Electrical Impedance Tomography of Human Brain Activity
Tidswell, T., Gibson, A. P., Bayford, R. H., & Holder, D. S. (2001) · NeuroImage · doi:10.1006/nimg.2000.0698 · Cited by 183 · see citing works
“These were: (1) The posterior quadrant of the EIT images, which corresponded to the visual cortex (Fox et al., 1986), or (2) The contralateral image quadrants to the moving or stimulated hand that corresponded to the contralateral motor (Kim et al., 1993) or somatosensory cortex (Ibanez et al.,…”
BackgroundMethodForward to the Past: The Case for Quantitative PET Imaging
Lammertsma, A. A. (2017) · Journal of Nuclear Medicine · doi:10.2967/jnumed.116.188029 · Cited by 177 · see citing works
“On the other hand, PET progressed into a more phenomenologic application, namely the detection of activated areas of CBF in the brain after a stimulus (22).”
BackgroundPiccinini, G. (2020) · doi:10.1093/oso/9780198866282.001.0001 · Cited by 176 · see citing works
Meta-Analysis in Human Neuroimaging: Computational Modeling of Large-Scale Databases
Fox, P. T., Lancaster, J. L., Laird, A. R., & Eickhoff, S. B. (2014) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062012-170320 · Cited by 172 · see citing works
“Although it was new to brain imaging, this strategy had been known to astronomers for centuries as “vernier acuity” and to vision scientists for decades as “hyperacuity” (Fox et al. 1986).”
Sadato, N., Ibañez, V., Campbell, G., Deiber, M., Bihan, D. L., & Hallett, M. (1997) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-199706000-00008 · Cited by 172 · see citing works
If neuroimaging is the answer, what is the question?
Kosslyn, S. M. (1999) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1999.0479 · Cited by 170 · see citing works
“For example, Fox et al. (1986) used PET to study the organization of Area 17 (primary visual cortex).”
MethodInfluentialCognitive neuroscience: Origins and promise.
Posner, M. I., & DiGirolamo, G. J. (2000) · Psychological Bulletin · doi:10.1037/0033-2909.126.6.873 · Cited by 166 · see citing works
Dynamic functional imaging of brain glucose utilization using fPET-FDG
Villien, M., Wey, H., Mandeville, J. B., Catana, C., Polimeni, J. R., Sander, C. Y. M., Zürcher, N. R., Chonde, D. B., Fowler, J. S., Rosen, B. R., et al. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.06.025 · Cited by 167 · see citing works
The Neuropsychology of the Prefrontal Cortex
Rezai, K., Andreasen, N. C., Alliger, R., Cohen, G., Swayze, V., & O'Leary, D. S. (1993) · Archives of Neurology · doi:10.1001/archneur.1993.00540060066020 · Cited by 247 · see citing works
Cells of the Blood–Brain Barrier: An Overview of the Neurovascular Unit in Health and Disease
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“Group averaging, however, was quickly validated in these first studies by showing that retinotopic mapping of the primary visual cortex occurred in response to a flashing checkerboard in the appropriate visual field (Fox et al., 1986).”
Dynamic Magnetic Resonance Imaging of the Rat Brain during Forepaw Stimulation
Hyder, F., Behar, K. L., Martin, M. A., Blamire, A. M., & Shulman, R. G. (1994) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1994.81 · Cited by 157 · see citing works
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Cortical magnification and peripheral vision
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“Many studies have focused on assessment of the roles of various parameters characterizing this mechanism (Vanzetta and Grinvald, 1999; Ugurbil et al., 2000; Fox et al., 1986; Belliveau et al., 1991; Buxton et al., 1998; Feng et al., 2001; Hess et al., 2000).”
Yamashita, Y., Maki, A., & Koizumi, H. (2001) · Medical Physics · doi:10.1118/1.1373401 · Cited by 139 · see citing works
Brain-imaging studies of cognitive functions
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A motion area in human visual cortex.
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Images of the Mind: Studies with Modern Imaging Techniques
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Brain Glucose Metabolism in Postanoxic Syndrome
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- Authors
- Fox, P. T., Mintun, M. A., Raichle, M. E., Miezin, F. M., Allman, J. M., & Van Essen, D. C.
- Affiliations
- Washington University in St. Louis (US)
- California Institute of Technology (US)
- Venue
- Nature
- Published
- 1986-10
- Volume
- 323
- Issue
- 6091
- Pages
- 806-809
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W1994364310
- Cited by
- 422
- References
- 22
- Citations by year
- 2026: 2 · 2025: 7 · 2024: 3 · 2023: 2 · 2022: 4 · 2021: 5 · 2020: 19 · 2019: 6 · 2018: 1 · 2017: 5 · 2016: 6 · 2015: 7 · 2014: 9 · 2013: 9 · 2012: 8
- FWCI
- 12.67
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- Topics
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Medical Imaging Techniques and Applications
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
- Keywords
- functional brain mapping, primary visual cortex, regional cerebral blood flow, positron emission tomography, spatial resolution, image subtraction, visual cortex
- MeSH terms
- Cerebrovascular Circulation, Humans, Image Enhancement, Regional Blood Flow, Subtraction Technique, Tomography, Emission-Computed, Visual Cortex
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