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Articles, Behavioral/Systems/Cognitive

Rapid Interactions between the Ventral Visual Stream and Emotion-Related Structures Rely on a Two-Pathway Architecture

David Rudrauf, Olivier David, Jean-Philippe Lachaux, Christopher K. Kovach, Jacques Martinerie, Bernard Renault and Antonio Damasio
Journal of Neuroscience 12 March 2008, 28 (11) 2793-2803; DOI: https://doi.org/10.1523/JNEUROSCI.3476-07.2008
David Rudrauf
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Olivier David
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Jean-Philippe Lachaux
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Christopher K. Kovach
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Jacques Martinerie
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Bernard Renault
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Antonio Damasio
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    Figure 1.

    Protocol and stimulus emotional competence. a, Protocol: randomized presentation of neutral, unpleasant, or pleasant movies based on static pictures (n = 3 × 60) during MEG recordings, followed after each trial by subjective ratings, including arousal and valence. b, Left, Pattern of average ratings of arousal and valence across subjects for each movie. Top right, Modulation of heart rate change by stimulus emotional competence. Bottom right, Correlation of valence with heart rate change. All results follow an expected pattern.

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    Figure 2.

    Tested models. a, Basic components of the generic model, including all the possible types of connections used in this report, within and between two connected regions. Top, Cortical regions are modeled as three layered columns with three types of neuronal populations (pyramidal, excitatory spiny, and inhibitory interneurons), connected through intrinsic and extrinsic (feedforward and backward) connections. Bottom, The dynamics is mathematically expressed at the level of neural populations and is defined by nonlinear differential equations in which the change of state of each unit dxi/dt depends on its current state xi(t); thalamic inputs ui(t); average firing rate of afferents S(xj(t − δij)); transmission delays δij; forward, backward, and intrinsic effective connectivity matrices CF, CB, Ci, and other parameters. The MEG signal M is assumed to be related to the local average current density x generated by pyramidal populations through a linear forward model M = GX (David et al., 2006). b, Lateral, mesial, and ventral views of the mapping of the regions of interest common to all models on a reference cortical tessellation [for color code, see text and c (top row)]. c, Schematic representation of the architecture of the tested models. All the models share the same basic layout (see text). Null model, Simple feedforward model. Model 1, Adjunction of connectivity modulation. Model 2 (2-stage model), Adjunction of local feedbacks. Model 3 (2-stage model), Adjunction of long-range feedbacks from structures of the AAS. Model 4 (2-pathway model), Adjunction of a direct subcortical retinotectal short-cut pathway to the AAS. Model 5 (2-pathway model), Alternative short-cut pathways to the AAS via the inferior longitudinal and frontal–occipital fasciculi. Model 6 (2-pathway model), Combination of models 4 and 5. Orange circles, “Synapses” at which modulation by emotional competence of the stimuli is implemented.

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    Figure 3.

    Basic MEG results. a, MEG evoked response averaged across stimulus and across subjects (n = 15) per category. b, Cortical noise normalized minimum-norm source reconstruction results averaged across subjects and thresholded above three SDs above baseline for each category. The results show an overall propagation of activity from early visual cortices to frontal regions through the temporal lobes, with indication of early responses in the OFC for unpleasant and pleasant stimuli. c, Thresholded minimum-norm results for the contrast between pleasant and neutral stimuli on slightly unfolded cortical surfaces. Effects are reconstructed in occipital and temporal regions, in the temporal pole and the OFC (early and late). Similar but less extended effects were found with unpleasant stimuli (see supplemental Fig. 1, available at www.jneurosci.org as supplemental material).

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    Figure 4.

    Dynamic causal modeling results. a, Log evidence (BIC) of the different models (log evidence of the null model subtracted). Left, Group level. The log evidence is significantly different between two-stage and two-pathway models according to Bayesian inference (Penny et al., 2004). Right, Individual level. For 13 of the 15 subjects, the two-pathway models have better log evidence than the other models. b, Time courses of the average (n = 15) absolute values of the evoked dynamics estimated at the level of the populations of pyramidal neurons, for each region of interest and model. c, Region color codes correspond to the color codes in Figure 2, b and c. The main traces (underlined by darker surfaces) correspond to the neutral condition. The secondary traces (underlined by lighter surfaces) correspond to the maximum average response to either pleasant or unpleasant stimuli. Black vertical bars indicate significant effects of modulation by emotional competence (p < 0.05 uncorrected) (see Materials and Methods).

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The Journal of Neuroscience: 28 (11)
Journal of Neuroscience
Vol. 28, Issue 11
12 Mar 2008
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Rapid Interactions between the Ventral Visual Stream and Emotion-Related Structures Rely on a Two-Pathway Architecture
David Rudrauf, Olivier David, Jean-Philippe Lachaux, Christopher K. Kovach, Jacques Martinerie, Bernard Renault, Antonio Damasio
Journal of Neuroscience 12 March 2008, 28 (11) 2793-2803; DOI: 10.1523/JNEUROSCI.3476-07.2008

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Rapid Interactions between the Ventral Visual Stream and Emotion-Related Structures Rely on a Two-Pathway Architecture
David Rudrauf, Olivier David, Jean-Philippe Lachaux, Christopher K. Kovach, Jacques Martinerie, Bernard Renault, Antonio Damasio
Journal of Neuroscience 12 March 2008, 28 (11) 2793-2803; DOI: 10.1523/JNEUROSCI.3476-07.2008
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