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Research Article

Functional magnetic resonance microscopy at single-cell resolution in Aplysia californica

Guillaume Radecki, Romuald Nargeot, Ileana Ozana Jelescu, Denis Le Bihan, and Luisa Ciobanu
  1. aNeuroSpin, Commissariat à l'Energie Atomique et aux Energies Alternatives, 91191 Gif-sur-Yvette, France; and
  2. bUniversité de Bordeaux and
  3. cCentre National de la Recherche Scientifique, Institut de Neurosciences Cognitives et Intégratives d'Aquitaine, Unité Mixte de Recherche 5287, F-33000 Bordeaux, France

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PNAS first published May 28, 2014; https://doi.org/10.1073/pnas.1403739111
Guillaume Radecki
aNeuroSpin, Commissariat à l'Energie Atomique et aux Energies Alternatives, 91191 Gif-sur-Yvette, France; and
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Romuald Nargeot
bUniversité de Bordeaux and
cCentre National de la Recherche Scientifique, Institut de Neurosciences Cognitives et Intégratives d'Aquitaine, Unité Mixte de Recherche 5287, F-33000 Bordeaux, France
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Ileana Ozana Jelescu
aNeuroSpin, Commissariat à l'Energie Atomique et aux Energies Alternatives, 91191 Gif-sur-Yvette, France; and
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Denis Le Bihan
aNeuroSpin, Commissariat à l'Energie Atomique et aux Energies Alternatives, 91191 Gif-sur-Yvette, France; and
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Luisa Ciobanu
aNeuroSpin, Commissariat à l'Energie Atomique et aux Energies Alternatives, 91191 Gif-sur-Yvette, France; and
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  • For correspondence: luisa.ciobanu@cea.fr
  1. Edited by John G. Hildebrand, University of Arizona, Tucson, AZ, and approved May 8, 2014 (received for review March 4, 2014)

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Significance

The direct observation with MRI of neuronal activity at single-neuron resolution represents a significant advancement in magnetic resonance (MR) microscopy and functional neuroimaging. The vast majority of high-resolution MR microscopy studies remain restricted to the generation of static images. This study shifts the focus of MR microscopy from noninvasive static imaging to dynamic investigations of activity in single cells and neuronal networks. Although most functional neuroimaging investigations are limited to averaging the signal from clusters of hundreds of neurons, we show that we are able to record the activity coming from individual neurons and their responses to sensory stimuli.

Abstract

In this work, we show the feasibility of performing functional MRI studies with single-cell resolution. At ultrahigh magnetic field, manganese-enhanced magnetic resonance microscopy allows the identification of most motor neurons in the buccal network of Aplysia at low, nontoxic Mn2+ concentrations. We establish that Mn2+ accumulates intracellularly on injection into the living Aplysia and that its concentration increases when the animals are presented with a sensory stimulus. We also show that we can distinguish between neuronal activities elicited by different types of stimuli. This method opens up a new avenue into probing the functional organization and plasticity of neuronal networks involved in goal-directed behaviors with single-cell resolution.

  • neuroimaging
  • manganese-enhanced MRI

Footnotes

  • ↵1To whom correspondence should be addressed. E-mail: luisa.ciobanu{at}cea.fr.
  • Author contributions: R.N., D.L.B., and L.C. designed research; G.R., I.O.J., and L.C. performed research; G.R., R.N., and L.C. analyzed data; and R.N. and L.C. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1403739111/-/DCSupplemental.

Freely available online through the PNAS open access option.

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Functional MRI at single-cell resolution
Guillaume Radecki, Romuald Nargeot, Ileana Ozana Jelescu, Denis Le Bihan, Luisa Ciobanu
Proceedings of the National Academy of Sciences May 2014, 201403739; DOI: 10.1073/pnas.1403739111

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Functional MRI at single-cell resolution
Guillaume Radecki, Romuald Nargeot, Ileana Ozana Jelescu, Denis Le Bihan, Luisa Ciobanu
Proceedings of the National Academy of Sciences May 2014, 201403739; DOI: 10.1073/pnas.1403739111
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