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Articles, Behavioral/Cognitive

Load Dependence of β and γ Oscillations Predicts Individual Capacity of Visual Attention

Sateri Rouhinen, Jonatan Panula, J. Matias Palva and Satu Palva
Journal of Neuroscience 27 November 2013, 33 (48) 19023-19033; DOI: https://doi.org/10.1523/JNEUROSCI.1666-13.2013
Sateri Rouhinen
1Neuroscience Center, University of Helsinki, 00014 Helsinki, Finland, and
2BioMag Laboratory, HUS Medical Imaging Center, Helsinki University Central Hospital, 00029 Helsinki, Finland
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Jonatan Panula
1Neuroscience Center, University of Helsinki, 00014 Helsinki, Finland, and
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J. Matias Palva
1Neuroscience Center, University of Helsinki, 00014 Helsinki, Finland, and
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Satu Palva
1Neuroscience Center, University of Helsinki, 00014 Helsinki, Finland, and
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  • Figure 1.
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    Figure 1.

    Experimental design and behavioral performance. A, In T1, the subjects were instructed to attend one to four moving pink discs and to detect brief (∼100 ms) changes in their shape (mouth openings). The example video frame is from a three-object condition. B, In T2, the subjects attended only the pink discs and ignored the yellow. The number of discs presented was always four, whereas the number of attended pink discs varied from one to four. Here, the example is from a two-object condition with the object in bottom exhibiting the shape during the target event. C, An example of paths along which the objects moved. D, E, The HRs and RTs decreased with an increasing number of attended objects in both T1 (D) and T2 (E). F, G, The overall magnitude of eye movements and the magnitude of fast (saccadic) movements were quantified with eye motion index (EMI) and saccade motion index (SMI), respectively. H, A schematic of the analysis design. Time window used for the analyses of oscillation amplitudes was 700–200 ms before the occurrence of target events. The horizontal lines indicate significantly different pairs (p < 0.05, Bonferroni corrected, N = 6). Error bars indicate SEM.

  • Figure 2.
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    Figure 2.

    Oscillation amplitude modulations are correlated with target detection and RT. A, In T1, detected target events were preceded by smaller oscillation amplitudes in θ- and β-bands than the missed target events. The y-axis displays the fraction of brain regions that had significantly larger (P+) or smaller (P−) mean oscillation amplitudes between the trials with correctly detected and missed target events. B, The oscillation amplitudes in the α-band were decreased in distributed occipital, frontal, and temporal regions and medial cortical regions. Amplitudes are displayed in inflated cortical surface from a medial (left) and lateral (right) views. The color scale shows the fractions of negative (blue, P−) and positive (red, P+) significant observations in the frequency band of interest (see color scale in lower right corner). C, In T2, detected targets were preceded by smaller oscillation amplitudes in θ- and α-bands than undetected targets. D, Αmplitude suppression was observed in the cingulate, insula, and visual cortical regions in OC and TC. E, In T1, oscillation amplitudes are correlated negatively with the RTs in θ-, β-, and γ-bands, hence indicating that stronger amplitudes predicted slower performance (greater RTs). F, Negative correlations with amplitudes and RTs were observed in SM regions, LPFC, including FEFs as well as in the medial cortical regions in cingulate and insula. The color scale indicates the fractions of significant positive and negative correlations. G, In T2, oscillation amplitudes were correlated positively with the RTs in β- and γ-bands, indicating that greater pretarget amplitudes predicted faster performance (smaller RTs). H, Positive correlations of oscillation amplitudes and RTs were observed across visual regions in OC, TC, and in PPC. I, Colored landmark labels. A, Anterior; m, middle; p, posterior; s, superior; i, inferior; C, central; D, dorsal; F, frontal; G, gyrus; J, junction; L, lateral; M, medial; O, occipital; P, parietal; S, sulcus; T, temporal; V, ventral; caS, calcarine sulcus; Ci, cingulated; FEF, frontal eye field (putative); IN, insula; IPS, intraparietal sulcus and transparietal; orb, orbital; orbSme, orbital sulcus and medial olfactory; som, somatomotor; PC, parietal cortex; PFC, prefrontal cortex; PPC, posterior parietal cortex (includes intraparietal sulcus [IPS] and superior parietal gyrus [sPG]); Vis, early visual areas (∼V1–V4, blue circle).

  • Figure 3.
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    Figure 3.

    Attentional load modulates oscillation amplitudes similarly in T1 and T2. A, In T1, increasing attentional load suppressed oscillation amplitudes in α- and β-bands and enhanced γ-band amplitudes. B, Amplitudes were decreased in widespread OC, TC, and PC cortical regions but also in FEF, LPFC, and medial cortical structures. The color scale indicates the fractions of significant positive and negative correlations in the frequency bands of interest (Fig. 2). C, In T2, attentional load strengthened oscillation amplitudes in the γ-band, whereas amplitudes in the α and β bands were only slightly suppressed. D, Oscillation amplitudes in the γ-band were strengthened extensively in the ventral LPFC and also in PPC, TPJ, and cingulate. See Figure 2 for abbreviations.

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    Figure 4.

    Attentional load modulates oscillation amplitudes differently in high- and low-capacity subjects. A, Individual capacity values in T1 for each subject and load condition were obtained by multiplying the target detection accuracy (HR) with the number of attended objects. The x-axis denotes the number of attended objects (N) (i.e., the attentional load). Red represents subjects with highest mean capacity in T1 and T2; blue represents those with lowest capacity. The values were used to divide the subjects into high-capacity (warmer colors) and low-capacity subjects (colder colors) (see Materials and Methods). B, In T1, attentional load strengthened γ-band amplitudes for high-capacity (solid lines) but not for low-capacity (dashed lines) subjects and suppressed the α- and β-band amplitudes differentially for high- and low-capacity subjects, respectively (Pearson's r < 0.01, FDR-corrected). These differences between groups were largely significant (gray line: two-way ANOVA, group × load interaction, p < 0.05, FDR-corrected). C, In high-capacity subjects, γ-band amplitudes were strengthened in the visual regions in OC, TC, LPFC, as well as in cingulate and orbital areas, whereas in the low-capacity subject group, these load-dependent modulations were absent. Amplitude suppression in α- and β-bands was observed in distributed areas in PPC, LPFC, and in medial cortical structures as in cingulate and insula. The color scale is as in Figure 2. D, Individual capacity values for T2 with the same subject-specific colors as in A. E, In T2, attentional load increased γ-band amplitudes both in high- and low-capacity subject groups (Pearson's r < 0.01, FDR-corrected), although the modulation was greater in the high-capacity subjects (two-way ANOVA, group × load interaction, p < 0.05, FDR-corrected) and decreased slightly α- and β-band amplitudes. F, In low-capacity subjects, α-band suppression was observed in medial cortical structures specifically in cingulate in which the amplitude suppression in high-capacity subjects was not as pronounced. In both low- and high-capacity subjects, γ-band amplitudes were load-dependently strengthened in the LPFC.

  • Figure 5.
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    Figure 5.

    Attentional load-dependent modulation of γ-band amplitudes is correlated with individual attentional capacity. A, Individual capacity values in T1 (see Fig. 4A) were used as the regressand in a correlation analysis after detrending with population mean performance, individual zero-meaning, and normalization to unit area under curve at the population level (see Materials and Methods). The y-axis displays the normalized capacity values. B, In T1, θ- and α-band suppression and the strengthening of β- and γ-band amplitudes with attentional load were correlated with individual attentional capacity. C, The load-dependently strengthened γ-band amplitudes were correlated with individual capacity limitations in several visual cortical regions in OC, TC, and PPC but also in distributed regions of LPFC and in cingulate and insula. D, Normalized capacity values for T2 as in A. E, In T2, load-dependent increase in oscillation amplitudes in all frequency bands was correlated positively with individual capacity. F, In θ–α-bands, positive correlations originated mainly from distributed visual regions in OC and TC and from PPC. In β- and γ-bands, the correlations between attentional capacity and load-dependent modulations were also observed in SM and throughout the LPFC.

  • Figure 6.
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    Figure 6.

    Oscillation amplitudes are greater in T2 than in T1 in all frequency bands. A, T2 was associated with stronger oscillation amplitudes than T1 (task effect of the two-way ANOVA for task × load p < 0.01, FDR-corrected). B, The stronger amplitudes in T2 originated from distributed visual regions mainly in temporal cortices as well as from distributed regions in LPFC.

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    Figure 7.

    Summary of the main results reveals that oscillation amplitudes are differentially modulated by task demands in early and late regions of visual processing hierarchy. A, Total fraction of positive significance in load and capacity conditions (Figs. 3 and 5) shown in inflated cortical surface. Pink, yellow, green, orange, and blue lines indicate LPFC, somatomotor (SM), PPC, TPJ, and visual ROIs, respectively. B, Pearson correlation coefficients (r) for the correlation of oscillation amplitudes with load, capacity, and decreasing reaction time (red, black, and green lines). Blue lines denote the difference of relative oscillation amplitudes (rA) between detected and undetected trials.

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The Journal of Neuroscience: 33 (48)
Journal of Neuroscience
Vol. 33, Issue 48
27 Nov 2013
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Load Dependence of β and γ Oscillations Predicts Individual Capacity of Visual Attention
Sateri Rouhinen, Jonatan Panula, J. Matias Palva, Satu Palva
Journal of Neuroscience 27 November 2013, 33 (48) 19023-19033; DOI: 10.1523/JNEUROSCI.1666-13.2013

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Load Dependence of β and γ Oscillations Predicts Individual Capacity of Visual Attention
Sateri Rouhinen, Jonatan Panula, J. Matias Palva, Satu Palva
Journal of Neuroscience 27 November 2013, 33 (48) 19023-19033; DOI: 10.1523/JNEUROSCI.1666-13.2013
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Keywords

  • MEG
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