The NIH experience in first advancing fMRI

doi:10.1016/j.neuroimage.2011.07.074

NeuroImage

Volume 62, Issue 2, 15 August 2012, Pages 632-636

https://doi.org/10.1016/j.neuroimage.2011.07.074 Get rights and content

Abstract

The introduction of functional MRI at NIH in 1992 was the outcome of research goals first formulated by Turner in 1983. Between 1988 and 1990, Turner worked at NIH on actively-shielded gradient coils and the implementation of EPI-based techniques, especially diffusion-weighted EPI. His work on hypoxia in cat brain in 1990 directly inspired Ken Kwong's demonstration of BOLD contrast in humans at MGH in May 1991. Turner collaborated actively with this MGH team, the first group to map entirely noninvasively human brain activity due to visual stimulation. He introduced BOLD fMRI at NIH in February 1992. This paper reviews the steps that led up to BOLD EPI, and Turner's initial applications of BOLD fMRI at NIH.

Highlights

► Motivation for investigation of BOLD contrast. ► Value of EPI data acquisition. ► Detailed chronology of first experiments. ► Response of NIH neuroscientists to successful BOLD fMRI.

Section snippets

Scientific context

My background is a BA degree in physics and mathematics, and a PhD in physics. After three years pursuing research into liquid metals and then liquid crystals as a physics postdoctoral fellow at the Cavendish Laboratory, Cambridge University, I left in 1975 to study social anthropology for two years at University College London. There I was taught that Western concepts of social behavior had little place in the interpretation of other cultures, which were considered to originate independently

Chronology

The original notebooks containing the key dates in this chronology between 1986 and 1993 are available in my personal library or on file at NIH.

The chronology is as follows:

1978: Turner read Lassen and Ingvar's Scientific American article on ¹³³Xe imaging of brain function.
1982: Turner was introduced to MRI at Edinburgh Royal Infirmary, Scotland.
1983: Turner viewed EPI movies of beating infant heart in Peter Mansfield's lab, Nottingham. Turner proposed EPI movies of brain function.
1986, 14th

History of BOLD at NIH

Joining NIH in 1988, I started work immediately with Denis Le Bihan, in the hopes that perfusion imaging using magnetic field gradient labeling of rapidly moving spins (IVIM) could identify regionally specific changes in cerebral blood flow (CBF). I implemented the technique of diffusion-weighted EPI, using a z-axis head gradient coil designed by me and built at NIH, on the 1.5 T GE Signa scanner at NIH. This was done with the help of James McFall, and the GE R&D engineers Joe Maier and Bob

Perspective

BOLD fMRI, using EPI data acquisition, is now the most common technique for mapping human brain activity. BOLD imaging unquestionably arose from observations in rat brain made by Seiji Ogawa, when he was a researcher at Bell Laboratories in New Jersey. He showed that gradient echo imaging, at the very high field strength of 7 Tesla, showed variations of visibility of rat brain veins that depended on the oxygenation level of the blood (Ogawa et al., 1990a, Ogawa et al., 1990b).

The MRI technique

References (37)

B.J. Casey et al.
Activation of prefrontal cortex in children during a nonspatial working memory task with functional MRI
Neuroimage
(1995)
H. Kuwabara et al.
Density of perfused capillaries in living human brain during functional activation
Prog. Brain Res.
(1992)
A. Prinster et al.
Simultaneous measurement of DeltaR2 and DeltaR2* in cat brain during hypoxia and hypercapnia
Neuroimage
(1997)
R. Turner
Gradient coil design: a review of methods
Magn. Reson. Imaging
(1993)
R. Turner et al.
Single-shot diffusion imaging at 2.0 Tesla
J. Magn. Reson.
(1990)
A.C. Zappe et al.
Direct measurement of oxygen extraction with fMRI using 6% CO2 inhalation
Magn. Reson. Imaging
(2008)
P.A. Bandettini et al.
Time course EPI of human brain function during task activation
Magn. Reson. Med.
(1992)
D. Bavelier et al.
Hemispheric specialization for English and ASL: left invariance-right variability
Neuroreport
(1998)
A.M. Blamire et al.
Dynamic mapping of the human visual cortex by high-speed magnetic resonance imaging
Proc. Natl. Acad. Sci. U. S. A.
(1992)
R.B. Buxton et al.
A model for the coupling between cerebral blood flow and oxygen metabolism during neural stimulation
J. Cereb. Blood Flow Metab.
(1997)

P.T. Fox et al.

Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects

Proc. Natl. Acad. Sci. U. S. A.

(1986)

J. Frahm et al.

Dynamic MR imaging of human brain oxygenation during rest and photic stimulation

J. Magn. Reson. Imaging

(1992)

K.J. Friston et al.

Analysis of functional MRI time series

Hum. Brain Mapp.

(1994)

R.D. Hoge et al.

Linear coupling between cerebral blood flow and oxygen consumption in activated human cortex

Proc. Natl. Acad. Sci. U. S. A.

(1999)

P. Jezzard et al.

Comparison of EPI gradient-echo contrast changes in cat brain caused by respiratory challenges with direct simultaneous evaluation of cerebral oxygenation via a cranial window

NMR Biomed.

(1994)

A. Karni et al.

Functional MRI evidence for adult motor cortex plasticity during motor skill learning

Nature

(1995)

A. Karni et al.

The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex

Proc. Natl. Acad. Sci. U. S. A.

(1998)

K.K. Kwong et al.

Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation

Proc. Natl. Acad. Sci. U. S. A.

(1992)

Cited by (4)

Functional-structural reorganisation of the neuronal network for auditory perception in subjects with unilateral hearing loss: Review of neuroimaging studies
2016, Hearing Research
Citation Excerpt :
One study utilized two different imaging methods (fMRI and T1 volumetric images). fMRI rests on the blood oxygenation level dependent (BOLD) contrast that gives an indirect measure of neuronal activity (Buxton, 2012; Ogawa et al., 1992; Kwong, 2012; Turner, 2012; Friston et al., 1996). The spatial distribution of the hyperoxygenation is therefore not necessarily directly comparable to the location of activated neurons (Scheffler et al., 1998).
This paper aims to provide a review of studies using neuroimaging to measure functional-structural reorganisation of the neuronal network for auditory perception after unilateral hearing loss.
A literature search was performed in PubMed. Search criterions were peer reviewed original research papers in English completed by the 11th of March 2015.
Twelve studies were found to use neuroimaging in subjects with unilateral hearing loss. An additional five papers not identified by the literature search were provided by a reviewer. Thus, a total of 17 studies were included in the review.
Four different neuroimaging methods were used in these studies: Functional magnetic resonance imaging (fMRI) (n = 11), diffusion tensor imaging (DTI) (n = 4), T1/T2 volumetric images (n = 2), magnetic resonance spectroscopy (MRS) (n = 1). One study utilized two imaging methods (fMRI and T1 volumetric images).
Neuroimaging techniques could provide valuable information regarding the effects of unilateral hearing loss on both auditory and non-auditory performance. fMRI-studies showing a bilateral BOLD-response in patients with unilateral hearing loss have not yet been followed by DTI studies confirming their microstructural correlates. In addition, the review shows that an auditory modality-specific deficit could affect multi-modal brain regions and their connections.
Twenty years of functional MRI: The science and the stories
2012, NeuroImage
Citation Excerpt :
Seiji Ogawa describes in a short piece his own experience of the beginnings of BOLD contrast in the context of human brain activation (Ogawa, 2012). Here, Ken Kwong (2012), Kamil Ugurbil (2012-a), myself (Bandettini, in 2012), Andrew Blamire (2012), and Bob Turner (2012), – five of the first six groups to successfully perform fMRI in the period between early 1991 and 1992 – each describe the story of their first BOLD fMRI experiments. How these accounts overlap and differ is truly a fascinating glimpse into these intense early and, as Mark Cohen of UCLA once said to me at an early meeting, “heady” days of fMRI.
Since its inception over twenty years ago, the field of functional magnetic resonance imaging (fMRI) has grown in usage, sophistication, range of applications, and impact. After twenty years, it's useful to briefly look back as well as forward — to size up just how far we have come and speculate just how far we may go. This is an introduction to the special issue of “Twenty years of fMRI: the science and the stories.” The one-hundred and three papers in this special issue highlight the major methodological developments and controversies of fMRI from a first person perspective over the past twenty years. The growth of this field is not just fascinating from a science and technology perspective, but also from a human perspective. Most who were fortunate enough to be part of this effort at the beginning, as well as those who jumped in along the way have their fair share of interesting stories consisting of top rate science as well as intense thought and effort, good or bad fortune, and some claim to a contribution. These stories are in the following papers, written by the current leaders in the field and the innovators throughout the twenty year history. The categories, designed to cover every aspect of the emergence and development of fMRI, include: pre-fMRI; the first BOLD brain activation results; developments in pulse sequences, imaging methods, and hardware for fMRI; methodological developments, issues, and mechanisms; new paradigm designs; education; and the future. Within this issue, we have a collage of overlapping, complementary, yet sometimes contradictory accounts of what happened during the breathtakingly diverse and intense development of this still growing field over the past twenty years.
Diagnostic capabilities of transcranial magnetic stimulation to predict motor recovery after a stroke
2020, Nervno-Myshechnye Bolezni
The physics of functional magnetic resonance imaging (fMRI)
2013, Reports on Progress in Physics

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ReviewThe NIH experience in first advancing fMRI

Abstract

Highlights

Section snippets

Scientific context

Chronology

History of BOLD at NIH

Perspective

Neuroimage

Prog. Brain Res.

Neuroimage

Magn. Reson. Imaging

J. Magn. Reson.

Magn. Reson. Imaging

Time course EPI of human brain function during task activation

Magn. Reson. Med.

Hemispheric specialization for English and ASL: left invariance-right variability

Neuroreport

Dynamic mapping of the human visual cortex by high-speed magnetic resonance imaging

Proc. Natl. Acad. Sci. U. S. A.

A model for the coupling between cerebral blood flow and oxygen metabolism during neural stimulation

J. Cereb. Blood Flow Metab.

Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects

Proc. Natl. Acad. Sci. U. S. A.

Dynamic MR imaging of human brain oxygenation during rest and photic stimulation

J. Magn. Reson. Imaging

Analysis of functional MRI time series

Hum. Brain Mapp.

Linear coupling between cerebral blood flow and oxygen consumption in activated human cortex

Proc. Natl. Acad. Sci. U. S. A.

Comparison of EPI gradient-echo contrast changes in cat brain caused by respiratory challenges with direct simultaneous evaluation of cerebral oxygenation via a cranial window

NMR Biomed.

Functional MRI evidence for adult motor cortex plasticity during motor skill learning

Nature

The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex

Proc. Natl. Acad. Sci. U. S. A.

Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation

Proc. Natl. Acad. Sci. U. S. A.

Review
The NIH experience in first advancing fMRI