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Articles, Behavioral/Systems/Cognitive

How Silent Is Silent Reading? Intracerebral Evidence for Top-Down Activation of Temporal Voice Areas during Reading

Marcela Perrone-Bertolotti, Jan Kujala, Juan R. Vidal, Carlos M. Hamame, Tomas Ossandon, Olivier Bertrand, Lorella Minotti, Philippe Kahane, Karim Jerbi and Jean-Philippe Lachaux
Journal of Neuroscience 5 December 2012, 32 (49) 17554-17562; DOI: https://doi.org/10.1523/JNEUROSCI.2982-12.2012
Marcela Perrone-Bertolotti
1INSERM U1028-CNRS UMR5292, Brain Dynamics and Cognition Team, Lyon Neuroscience Research Center, F-69500 Lyon-Bron, France;
2University Claude Bernard, F-69000 Lyon, France;
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Jan Kujala
1INSERM U1028-CNRS UMR5292, Brain Dynamics and Cognition Team, Lyon Neuroscience Research Center, F-69500 Lyon-Bron, France;
2University Claude Bernard, F-69000 Lyon, France;
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Juan R. Vidal
1INSERM U1028-CNRS UMR5292, Brain Dynamics and Cognition Team, Lyon Neuroscience Research Center, F-69500 Lyon-Bron, France;
2University Claude Bernard, F-69000 Lyon, France;
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Carlos M. Hamame
3Laboratoire de Psychologie Cognitive, CNRS (UMR 6146), Aix-Marseille Université 13003 Marseille Cedex, 3 France;
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Tomas Ossandon
4Departamento de Psiquiatría, Facultad de Medicina y Centro Interdisciplinario de Neurociencia, Pontificia Universidad Católica de Chile, CL-8330024 Santiago, Chile; and
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Olivier Bertrand
1INSERM U1028-CNRS UMR5292, Brain Dynamics and Cognition Team, Lyon Neuroscience Research Center, F-69500 Lyon-Bron, France;
2University Claude Bernard, F-69000 Lyon, France;
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Lorella Minotti
5CHU Grenoble and Department of Neurology, INSERM U704, F-38043 Grenoble, France
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Philippe Kahane
5CHU Grenoble and Department of Neurology, INSERM U704, F-38043 Grenoble, France
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Karim Jerbi
1INSERM U1028-CNRS UMR5292, Brain Dynamics and Cognition Team, Lyon Neuroscience Research Center, F-69500 Lyon-Bron, France;
2University Claude Bernard, F-69000 Lyon, France;
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Jean-Philippe Lachaux
1INSERM U1028-CNRS UMR5292, Brain Dynamics and Cognition Team, Lyon Neuroscience Research Center, F-69500 Lyon-Bron, France;
2University Claude Bernard, F-69000 Lyon, France;
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Abstract

As you might experience it while reading this sentence, silent reading often involves an imagery speech component: we can hear our own “inner voice” pronouncing words mentally. Recent functional magnetic resonance imaging studies have associated that component with increased metabolic activity in the auditory cortex, including voice-selective areas. It remains to be determined, however, whether this activation arises automatically from early bottom-up visual inputs or whether it depends on late top-down control processes modulated by task demands. To answer this question, we collaborated with four epileptic human patients recorded with intracranial electrodes in the auditory cortex for therapeutic purposes, and measured high-frequency (50–150 Hz) “gamma” activity as a proxy of population level spiking activity. Temporal voice-selective areas (TVAs) were identified with an auditory localizer task and monitored as participants viewed words flashed on screen. We compared neural responses depending on whether words were attended or ignored and found a significant increase of neural activity in response to words, strongly enhanced by attention. In one of the patients, we could record that response at 800 ms in TVAs, but also at 700 ms in the primary auditory cortex and at 300 ms in the ventral occipital temporal cortex. Furthermore, single-trial analysis revealed a considerable jitter between activation peaks in visual and auditory cortices. Altogether, our results demonstrate that the multimodal mental experience of reading is in fact a heterogeneous complex of asynchronous neural responses, and that auditory and visual modalities often process distinct temporal frames of our environment at the same time.

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The Journal of Neuroscience: 32 (49)
Journal of Neuroscience
Vol. 32, Issue 49
5 Dec 2012
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How Silent Is Silent Reading? Intracerebral Evidence for Top-Down Activation of Temporal Voice Areas during Reading
Marcela Perrone-Bertolotti, Jan Kujala, Juan R. Vidal, Carlos M. Hamame, Tomas Ossandon, Olivier Bertrand, Lorella Minotti, Philippe Kahane, Karim Jerbi, Jean-Philippe Lachaux
Journal of Neuroscience 5 December 2012, 32 (49) 17554-17562; DOI: 10.1523/JNEUROSCI.2982-12.2012

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How Silent Is Silent Reading? Intracerebral Evidence for Top-Down Activation of Temporal Voice Areas during Reading
Marcela Perrone-Bertolotti, Jan Kujala, Juan R. Vidal, Carlos M. Hamame, Tomas Ossandon, Olivier Bertrand, Lorella Minotti, Philippe Kahane, Karim Jerbi, Jean-Philippe Lachaux
Journal of Neuroscience 5 December 2012, 32 (49) 17554-17562; DOI: 10.1523/JNEUROSCI.2982-12.2012
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