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Articles, Behavioral/Systems/Cognitive

Interactions of Top-Down and Bottom-Up Mechanisms in Human Visual Cortex

Stephanie McMains and Sabine Kastner
Journal of Neuroscience 12 January 2011, 31 (2) 587-597; https://doi.org/10.1523/JNEUROSCI.3766-10.2011
Stephanie McMains
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Sabine Kastner
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  • Figure 1.
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    Figure 1.

    Hypotheses for interactions of top-down and bottom-up processes to resolve neural competition. A, The spotlight hypothesis proposes that attentional modulation will be primarily additive regardless of the amount of neural competition that needs to be resolved. B, The interface hypothesis proposes that the amount of attentional modulation will dependent on the amount of neural competition that has not been resolved through bottom-up processes. Thus, the modulation will be strongest in cases without any perceptual organization and weakest in cases with strong perceptual organization.

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    Figure 2.

    Experimental design and visual stimuli. Four illusory contour inducers were presented under three display conditions: with the inducers rotated inward and with the same angle to form a strong illusory figure (A); with the inducers rotated inward, but the left two inducers and right two inducers having different angles, thereby forming a weak percept of an illusory figure (B); or with the inducers rotated outward so that no illusory figure was present (C). The stimulus display was presented in the upper right visual quadrant using two presentation conditions. D, In the sequential condition, each inducer was presented alone for 250 ms each. E, In the simultaneous condition, all four inducers were presented at the same time for 250 ms each. Each presentation period lasted 1 s, with 20 presentations in a peripheral stimulation block. On average, a stimulus appeared at each of the four locations every 750 ms. Presentation conditions and levels of perceptual organization were probed while subjects either performed a task at fixation (and ignored the peripheral stimuli), or attended to the peripheral stimuli and performed a task on the lower left inducer closest to fixation.

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    Figure 3.

    Mean signal changes and sensory suppression indexes for the unattended conditions. A, For each subject, area, and condition, mean signal changes were computed by averaging across the six peak time points of the fMRI time series. Group data were yielded by averaging across subjects (n = 10). In general, visually evoked activity was reduced for the SIM (filled bars) compared with the SEQ (open bars) conditions, reflecting the mutual suppression that occurs when multiple stimuli compete. In addition, modulations for just the UnATT SIM conditions varied monotonically with the amount of perceptual organization present in V2, V3, and V4. B, Sensory suppression indexes were calculated on the basis of mean signal changes [(SEQ − SIM)/(SEQ + SIM)]. SSIs in early visual cortex (V1, V2, V3) and area V4 of the ventral stream were largest when the stimuli were randomly arranged as in the NoGrp condition. As predicted, SSIs varied linearly with the strength of the perceptual grouping among the elements in the display in V2, V3, and V4. The vertical bars indicate SEM.

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    Figure 4.

    Mean signal changes for the unattended and attended conditions. For each subject, area, and condition, mean signal changes were computed by averaging across the six peak time points of the fMRI time series. Group data were yielded by averaging across subjects (n = 10). Mean signals are presented for V1, V2, V3, and V4. When subjects attended to the peripheral stimuli (gray and striped bars), activity throughout visual cortex increased compared with when subjects attended away from the peripheral stimuli and performed a task at fixation (white and black bars). The vertical bars indicate SEM.

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    Figure 5.

    Attentional modulation indexes for SEQ and SIM presentation conditions as a function of perceptual organization. Attentional modulation indexes [(ATT − UnATT)/(ATT + UnATT)] were calculated for each level of grouping for the SEQ (black lines) and SIM (gray lines) conditions. Consistent with the interface hypothesis, attentional modulation depended on display condition for SIM presented displays where competition among elements could occur, but not for the SEQ displays. For all visual areas, there was a significant linear relationship between attentional modulation and perceptual grouping for SIM displays. In addition, attentional modulation was generally larger for the SIM compared with the SEQ conditions. The vertical bars indicate SEM.

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    Figure 6.

    Sensory suppression indexes for the attended and unattended conditions as a function of perceptual organization. Sensory suppression indexes [(SEQ − SIM)/(SEQ + SIM)] were computed for attended (black dashed lines) and unattended (gray dashed lines) conditions for each level of grouping. Sensory suppression was reduced when subjects attended to the display compared with when subjects attended away from the displays. SSIs were reduced by the largest amount for the NoGrp displays and the smallest amount for the StrongGrp displays. The final amount of competition present when top-down attention and bottom-up perceptual grouping combined to counteract competition did not differ for the different display conditions (SSIsATT).

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    Figure 7.

    Correlations between sensory suppression and attention effects. Attentional modulation indexes from the SIM conditions (AMISIM) and sensory suppression indexes from the UnATT conditions (SSIUnATT) for each subject and level of grouping were correlated with the respective UnATT SIM to eliminate any inherent correlation because of the fact that each index contains the UnATT SIM condition. Next, the residuals were correlated to investigate the relationship between attention and sensory suppression effects. Values were plotted for the NoGrp (light gray circles), WeakGrp (gray squares), and StrongGrp (black diamonds) for all subjects, excluding outliers that fell >2 SDs away from the mean. A significant correlation between attentional modulation and sensory suppression effects was observed for all visual areas (V1–V3: t > 3.03, p < 0.01; V4: t = 2.35, p < 0.05). This suggests that the degree of attentional modulation within individual subjects is closely tied to the degree of competition for all levels of grouping.

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    Table 1.

    Accuracy and reaction time for behavioral task

    ConditionAccuracyRT (ms)
    UnATT SEQ NoGrp75 (3)548 (16)
    UnATT SIM NoGrp72 (4)553 (13)
    UnATT SEQ WeakGrp76 (3)544 (14)
    UnATT SIM WeakGrp73 (4)553 (14)
    UnATT SEQ StrongGrp74 (3)546 (15)
    UnATT SIM StrongGrp72 (4)554 (13)
    ATT SEQ NoGrp73 (1)489 (13)
    ATT SIM NoGrp70 (1)512 (19)
    ATT SEQ WeakGrp77 (2)485 (8)
    ATT SIM WeakGrp71 (1)507 (18)
    ATT SEQ StrongGrp79 (3)476 (8)
    ATT SIM StrongGrp73 (1)496 (17)
    • RT, Reaction time.

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The Journal of Neuroscience: 31 (2)
Journal of Neuroscience
Vol. 31, Issue 2
12 Jan 2011
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Interactions of Top-Down and Bottom-Up Mechanisms in Human Visual Cortex
Stephanie McMains, Sabine Kastner
Journal of Neuroscience 12 January 2011, 31 (2) 587-597; DOI: 10.1523/JNEUROSCI.3766-10.2011

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Interactions of Top-Down and Bottom-Up Mechanisms in Human Visual Cortex
Stephanie McMains, Sabine Kastner
Journal of Neuroscience 12 January 2011, 31 (2) 587-597; DOI: 10.1523/JNEUROSCI.3766-10.2011
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