Conscious and unconscious processing of nonverbal predictability in Wernicke's area

Abstract

The association of nonverbal predictability and brain activation was examined using functional magnetic resonance imaging in humans. Participants regarded four squares displayed horizontally across a screen and counted the incidence of a particular color. A repeating spatial sequence with varying levels of predictability was embedded within a random color presentation. Both Wernicke's area and its right homolog displayed a negative correlation with temporal predictability, and this effect was independent of individuals' conscious awareness of the sequence. When individuals were made aware of the underlying sequential predictability, a widespread network of cortical regions displayed activity that correlated with the predictability. Conscious processing of predictability resulted in a positive correlation to activity in right prefrontal cortex but a negative correlation in posterior parietal cortex. These results suggest that conscious processing of predictability invokes a large-scale cortical network, but independently of awareness, Wernicke's area processes predictive events in time and may not be exclusively associated with language.

Fig. 1.

Experimental design of the presented task. Four squares were displayed horizontally across a screen. The squares were individually illuminated in one of three randomly selected colors (blue, red, or yellow) for 1 sec. Beginning at 100, participants kept a mental count of the total number of blue squares presented during the entire session. The sequence of spatial positions illuminated was determined by an artificial grammar with the entropy of the sequence varying between condition blocks. The given example illustrates 4 sec of a scan where the spatial sequence was presented (1-3-2-4). The occurrence of functional scans and the subject's mental count of the blue squares are also shown.

Fig. 2.

Overall block design of the functional scan session. Each of the three entropy levels (0, 1, and 2) were presented three times during the course of the functional scan. Each entropy block lasted for 45 scans (90 sec).

Fig. 3.

Sagittal and transverse projections of the statistical comparison for the UNAWARE + AWARE, UNAWARE > AWARE, and AWARE > UNAWARE groups across all three entropy conditions. UNAWARE + AWARE shows regions common to both of these groups that positively correlated with entropy. The other two columns show the interaction of awareness and entropy. Horizontal linesin the sagittal images indicate planes displayed in Figure 4. All groups were analyzed with a significance threshold ofp < 0.01 (uncorrected).

Fig. 4.

Statistical parametric maps showing regions that correlated with conditional entropy. Transverse planes (Talairach,Z = +64, Z = +32, andZ = +8) for both the conjunction (UNAWARE + AWARE) and the interactions (UNAWARE > AWARE, AWARE > UNAWARE) between the groups. The relationship of the adjusted BOLD response to entropy is shown for selected regions in the AWARE, UNAWARE, and RANDOM groups (right). Wernicke's area (coordinates: −52, −20 to −40, 4–8) showed a significant correlation to entropy independent of awareness. The right posterior parietal cortex displayed a significant positive entropy relationship only in the AWARE group (coordinates: 28, -48, 64). The right prefrontal cortex displayed a negative relationship to entropy in the AWARE group (coordinates: 20, 24, 32). The RANDOM did not display any of these relationships.

Fig. 5.

Differing temporal effects between the RANDOM group (n = 5) and the SEQUENCE group (n = 5) in Wernicke's area (coordinates: −56, −28, 12). Activation decreased as the grammar statistics were acquired in the SEQUENCE group, but not in the RANDOM group (ANCOVA,p = 0.004).