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Articles, Behavioral/Systems/Cognitive

Long-Distance Amplitude Correlations in the High Gamma Band Reveal Segregation and Integration within the Reading Network

Juan R. Vidal, Samson Freyermuth, Karim Jerbi, Carlos M. Hamamé, Tomas Ossandon, Olivier Bertrand, Lorella Minotti, Philippe Kahane, Alain Berthoz and Jean-Philippe Lachaux
Journal of Neuroscience 9 May 2012, 32 (19) 6421-6434; DOI: https://doi.org/10.1523/JNEUROSCI.4363-11.2012
Juan R. Vidal
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Samson Freyermuth
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Karim Jerbi
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Carlos M. Hamamé
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Tomas Ossandon
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Olivier Bertrand
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Lorella Minotti
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Philippe Kahane
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Alain Berthoz
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Jean-Philippe Lachaux
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  • Figure 1.
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    Figure 1.

    Experimental design, ocular behavior, and electrode implantation. A, Depiction of the images and general time sequence used in the reading experiment. In each trial, a sentence was presented and patients were asked to scan through it from left to right and press a button when finished to subsequently perform the task (see Materials and Methods). B, Three illustrative examples of saccadic eye movements during sentence reading for each one of the three conditions termed semantic, phonological, and visual (see Materials and Methods). In the semantic condition, subjects had to read a real sentence and judge whether it belonged to an ongoing story. In the phonological condition, subjects had to form a global pronounceable character string from groups of identical letters and decide whether the global string was a word or a pseudoword. Subjects were explicitly instructed to form a mental auditory representation of the string, as it formed. In the visual condition, subjects had to determine whether there were more than two digits hidden in a string of random letters. English translation: Left panel, “The king has left his castle”; middle panel, “screen.” C, Histogram of saccade distribution in time after stimulus onset, for each one of the three conditions. D, The top panel depicts electrode implantation sites for all patients in a MNI brain, from left and right hemispheres, respectively. On the lower part, a coronal brain view shows an example of multiple contact sites of a single electrode in one patient.

  • Figure 2.
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    Figure 2.

    Recordings from MTG and SMG. A, Glass brain illustrating the recording sites for all patients concerned with the MTG and SMG clusters. B, Examples of single-trial average gamma-band amplitudes in (0:2000 ms) time window after stimulus onset, from two different recording sites. The amplitude value of each trial is plotted as a dot, in different color for each one of the three experimental conditions. C, Left panel, Group average of gamma-band amplitude (40–150 Hz) for the SEM, PHO, and VIS conditions, for the MTG recording sites across patients. Shaded regions indicate ±1SEM. Middle, Single-trial gamma-band amplitude responses in one patient, at an MTG recording site for patient 1. Right, Anatomical location of the recording site shown in the middle panel (Talairach coordinates: −53 −33 −4.4). D, Left panel, Group average of gamma-band amplitude (40–150 Hz) for the SEM, PHO, and VIS conditions, for the SMG recording sites across patients. Shaded regions indicate ±1SEM. Middle, Single-trial gamma-band amplitude responses at an SMG recording site for patient 2. Right, Anatomical location of the recording site shown in the middle panel (Talairach coordinates: −60 −22 25). E, Comparison of gamma-band responses from the same electrode in two different reading tasks in patient 4. Left panel, Single-trial gamma-band plot from the current sentence reading experiment showing dominant responses in the SEM condition. Middle, Single-trial gamma-band plot in a separate single-word reading task. There is no specific gamma-band response compared with baseline for meaningful words. Right, The Talairach coordinates from this recording site are as follows: (−53 −20 −8.4).

  • Figure 3.
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    Figure 3.

    Recordings from IFC clusters specific to semantic sentences (IFC SEM) and phonologic sentences (IFC PHO). A, Left panel, Average gamma-band amplitude across trials (40–150 Hz) for the SEM, PHO, and VIS conditions, for four recording sites in the prefrontal cortex of patient 4. Shaded regions indicate ±1SEM. Right, MRI located anatomical positions of the four recording sites. Talairach coordinates of recording sites from medial to lateral position on the electrode: (−44 5.7 12), (−48 5.7 12), (−52 5.7 12), (−55 5.7 12). B, Left panel, Group average of gamma-band amplitude (40–150 Hz) for the SEM, PHO, and VIS conditions for the IFC SEM cluster. The shaded regions indicate ±1SEM. Right, Single-trial gamma-band amplitude responses from the IFC SEM in patient 11. Sustained gamma-band activity is observed, mainly in the SEM condition. Single trials are ordered according to increased reaction time represented by white dots. C, Left panel, Group average of gamma-band amplitude (40–150 Hz) for the SEM, PHO, and VIS conditions for the IFC PHO cluster. The shaded regions indicate ±1SEM. Right, Single-trial gamma-band amplitude responses from the IFC PHO in patient 8. Sustained gamma-band activity is observed, mainly in the PHO condition. D, Glass brain illustrating the recording sites for all patients concerned with the IFC SEM and IFC PHO clusters.

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    Figure 4.

    Recordings from three ventral occipito-temporal cortex clusters (VOTC INT, VOTC MID, VOTC EXT). A, Group average of gamma-band amplitude (40–150 Hz) for the SEM, PHO, and VIS conditions within the three VOTC clusters. B, Glass brain illustrating the recording sites for all patients concerned with the three VOTC clusters. C, Top panel, MRI location of three recording sites. Bottom, Single-trial gamma-band amplitude responses for the three recording sites in VOTC. Gamma-band responses in the inner recording site show a clear amplitude increase in the semantic and phonological condition compared with the visual condition. In the external sites, the phonological condition shows the strongest gamma-band response. In all plots, single trials are ordered according to increased reaction time represented by white dots. Talairach coordinates of the three recording sites from medial to lateral position on the electrode are as follows: (−29 −43 −9.8), (−33 −43 −9.8), (−51 −43 −9.8).

  • Figure 5.
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    Figure 5.

    Long-range fronto-temporal gamma-band amplitude correlations during reading. A, Anatomical locations of two recordings sites, in the middle temporal gyrus (Talairach coordinates: −53 −33 −4.4) and in the inferior frontal cortex (Talairach coordinates: −43 31 −9.5) in one patient. B, Single-trial plots of each recording site are ordered according to increasing reaction times (white dots in plots). In both sites, there are more gamma-band responses in the SEM condition compared with the PHO and VIS conditions. C, Illustrative single-trial amplitude profiles from MTG and IFC elicited while reading one sentence. The correlation coefficient for this trial is r = 0.6. The sentence in French reads: “I will not have to wet my clothes to reach it.” D, The outcome of the statistics when comparing the trial-by-trial correlation coefficients to a surrogate distribution of correlation coefficients, for each condition. The y-axis represents a quantitative trial number value, normalized between 0 and 1.

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    Figure 6.

    Long-range gamma-band amplitude correlations during reading between fusiform gyrus and inferior frontal cortex. A, Anatomical locations of two recordings sites, in the fusiform gyrus (Talairach coordinates: −50 −45 −12) and in the inferior frontal cortex (Talairach coordinates: −41 38 13) in one patient. B, Single-trial plots of each recording site are ordered according to increasing reaction times (white dots in plots). In both sites, there are more gamma-band responses in the SEM condition compared with the PHO and VIS conditions. C, Illustrative single-trial amplitude profiles from FG and IFC elicited while reading one sentence. The correlation coefficient for this trial is r = 0.62. The sentence reads: “He was an orphan and lived alone with his mother.” D, The outcome of the statistics when comparing the trial-by-trial correlation coefficients to a surrogate distribution of correlation coefficients, for each condition. The y-axis represents a quantitative trial number value, normalized between 0 and 1.

  • Figure 7.
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    Figure 7.

    Illustrative gamma-band amplitude anticorrelation during reading between angular gyrus and fusiform gyrus. A, Anatomical locations of two recordings sites, in the angular gyrus (Talairach coordinates: −53 −39 31) and in the fusiform gyrus (Talairach coordinates: −33 −51 −17) in one patient. B, Single-trial plots of each recording site are ordered according to increasing reaction times (white dots in plots). Gamma-band responses in the angular gyrus systematically decrease for SEM and PHO conditions compared with baseline. In the fusiform gyrus, gamma-band responses increase in both SEM and PHO conditions compared with baseline. C, Illustrative example of gamma-band amplitude behavior in consecutive trials at both recording sites during sentence reading. D, The outcome of the statistics when comparing the trial-by-trial correlation coefficients to a surrogate distribution of correlation coefficients, for each condition. The y-axis represents a quantitative trial number value, normalized between 0 and 1. Single-trial correlation coefficients for gamma-band responses tend to be negative between recorded angular gyrus and fusiform gyrus, in both SEM and PHO conditions.

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    Figure 8.

    Fragmentation of the reading network. A, Red (blue, respectively) dots indicate sites with the strongest response in the semantic (phonological, respectively) condition. The green dots indicate sites with equally strong response in both conditions. The figure only shows sites selected for the correlation analysis (see Results). Positions are displayed in the y,z MNI space (3-D model of the MNI single-subject brain; microGL; www.mricro.com). In the top panel, the white lines connect sites with significant correlation in either condition. In the middle panel, the red lines connect sites with a stronger correlation in SEM than in PHO or VIS (Kruskal–Wallis, p < 0.05). In the bottom panel, the blue lines connect sites with a stronger correlation in condition PHO than in conditions SEM or VIS. B, Individual plots show examples of single-trial gamma amplitude. These signals, from two distant recording sites, correlated during condition PHO and during condition SEM (sites indicated by square boxes). Left panel, Two recordings sites (patient 1) are fusiform gyrus (blue) and inferior frontal gyrus (red). Right panel, The two recording sites (patient 8) are in the middle temporal gyrus (blue) and in the inferior frontal cortex (red).

Tables

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    Table 1.

    Patients' demographics

    PatientGenderAgeHandednessVerbal IQHemispheric lateralization for languageSeizure onset zone
    1F43RH87LeftLeft anterior entorhinal cortex
    2M51RH96LeftLeft anterior temporal lobe
    3F38RH98NDLeft anterior temporal lobe
    4F35RH96NDRight insula and anterior temporal cortex
    5F33RHNDNDLeft hippocampus
    6F56AM104LeftLeft medial temporal lobe
    7F26RHNDNDLeft precentral gyrus
    8F46RH101LeftLeft anterior hippocampus/temporal pole
    9F23LH101Bilateral (L > R)Right anterior frontal cortex
    10M23RH105NDLeft posterior temporal cortex
    11F22RH101LeftLeft hippocampus
    12F24LH83Bilateral (R > L)Left temporal pole/hippocampus
    • Patients' descriptives include gender, age, handedness, verbal IQ, hemispheric lateralization for language assessed by fMRI, and seizure onset zone. RH, Right-handed; LH, left-handed; AM, ambidextrous; ND, not done.

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    Table 2.

    Effects of electrical cortical stimulations at 50 Hz

    ROIElectrodePatientElectric stimulation mapping responses
    MTGe′61Heavy weight feeling rising from legs to stomach (1 mA)
    MTGu′56Feels like gravel in the head, not auditory (1 mA)
    MTGu′66Feels like gravel in the head, not auditory (1 mA)
    SMGs′92Hard to find words to talk (2 mA); trouble reading (3 mA)
    SMGs′102Hard to find words to talk (2 mA); trouble reading (3 mA)
    SMGs′75Trouble pronouncing words when reading (0.8 mA)
    SMGs′85Trouble pronouncing words when reading (0.8 mA)
    PFC PHOq′66Wants to move left hand (1 mA)
    PFC PHOq′76Wants to move left hand (1 mA)
    PFC PHOr′87Paresthesis of right inferior hemi-face (1.6 mA)
    PFC PHOr′97Paresthesis of right inferior hemi-face (1.6 mA)
    VOTC INTf′21Searching for words during speech (1–3 mA)
    VOTC INTf′25Trouble reading; had to decompose words to read them (2 mA)
    VOTC MIDf′35Trouble reading; had to decompose words to read them (2 mA)
    VOTC MIDf′411Right hemifield visual illusion (1 mA)
    VOTC EXTf′71Searching for words during speech (1–3 mA)
    VOTC EXTf′81Searching for words during speech (1–3 mA)
    VOTC EXTe′72Trouble reading (3 mA)
    VOTC EXTe84Body tilts to the side L > R (1 mA)
    • The patient's response is reported for each electrode in region of interest (ROI). Electrical stimulation was applied for maximum 5 s at varying intensities, ranging from 0.8 to 3 mA.

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The Journal of Neuroscience: 32 (19)
Journal of Neuroscience
Vol. 32, Issue 19
9 May 2012
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Long-Distance Amplitude Correlations in the High Gamma Band Reveal Segregation and Integration within the Reading Network
Juan R. Vidal, Samson Freyermuth, Karim Jerbi, Carlos M. Hamamé, Tomas Ossandon, Olivier Bertrand, Lorella Minotti, Philippe Kahane, Alain Berthoz, Jean-Philippe Lachaux
Journal of Neuroscience 9 May 2012, 32 (19) 6421-6434; DOI: 10.1523/JNEUROSCI.4363-11.2012

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Long-Distance Amplitude Correlations in the High Gamma Band Reveal Segregation and Integration within the Reading Network
Juan R. Vidal, Samson Freyermuth, Karim Jerbi, Carlos M. Hamamé, Tomas Ossandon, Olivier Bertrand, Lorella Minotti, Philippe Kahane, Alain Berthoz, Jean-Philippe Lachaux
Journal of Neuroscience 9 May 2012, 32 (19) 6421-6434; DOI: 10.1523/JNEUROSCI.4363-11.2012
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