Complementary hemispheric specialization for language production and visuospatial attention

Abstract

Language production and spatial attention are the most salient lateralized cerebral functions, and their complementary specialization has been observed in the majority of the population. To investigate whether the complementary specialization has a causal origin (the lateralization of one function causes the opposite lateralization of the other) or rather is a statistical phenomenon (different functions lateralize independently), we determined the lateralization for spatial attention in a group of individuals with known atypical right hemispheric (RH) lateralization for speech production, based on a previous large-scale screening of left-handers. We show that all 13 participants with RH language dominance have left-hemispheric dominance for spatial attention, and all but one of 16 participants with left-hemispheric language dominance are RH dominant for spatial attention. Activity was observed in the dorsal fronto-parietal pathway of attention, including the inferior parietal sulcus and superior parietal lobule, the frontal eye-movement field, and the inferior frontal sulcus/gyrus, and these regions functionally colateralized in the hemisphere dominant for attention, independently of the side of lateralization. Our results clearly support the Causal hypothesis about the complementary specialization, and we speculate that it derives from a longstanding evolutionary origin. We also suggest that the conclusions about lateralization based on an unselected sample of the population and laterality assessment using coarse functional transcranial Doppler sonography should be interpreted with more caution.

Fig. 1.

Language production and visuospatial attention lateralize to different hemispheres, independent of the side of lateralization. Results for participants with (A) typical lateralization or (B) atypical lateralization, for word generation (in blue, word generation against repetition) and for the Landmark task (in green, Landmark against control task). In each panel the left picture shows activation in the left hemisphere, and the middle picture shows activation in the right hemisphere. The group level activations are rendered on the brain of a single participant with typical lateralization, with values of t > 4.98 (P < 0.0001 uncorrected) for the typical group (n = 15) and t > 4.30 (P < 0.001 uncorrected) for the atypical group (n = 13). The right picture in each panel shows the outcome of the additional interhemispheric difference analysis for the Landmark task (in red-yellow-blue, Landmark against control task).

Fig. 2.

Lateralization patterns for all 29 participants. The red diamonds show the outcome of the comparison of LM and LMC in IPS/SPL with the inferior frontal lateralization of language production (Word generation > Control). All but one participant had language production and spatial attention lateralized to opposite hemispheres, no matter whether the lateralization pattern was typical or atypical (15 participants showed the typical LH language–RH attention pattern, and 13 participants showed the atypical RH language–LH attention pattern). The blue triangles show the outcome of the analysis when the laterality index of the Landmark task is based on a comparison of LM and Rest. This analysis gives less clear data.

Fig. 3.

Lateralization patterns of visuospatial attention in the Landmark task (in green, Landmark against control task), and right-lateralized activations common to the LM and the LMC (in red, both against Rest condition). All participants are left-handed, either (A) with typical lateralization or (B) with atypical lateralization, and responses were made with the left hand. (A) Fifteen participants with typical lateralization. (B) Thirteen participants with atypical lateralization.

Fig. 4.

The laterality of frontal (FEF and IFS) and occipital activations are correlated to the laterality of parietal (IPS/SPL) activations in the Landmark task.

Fig. P1.

Language production and visuospatial attention lateralize to different hemispheres. (A) Participants with typical language lateralization (blue, word generation against repetition; green, Landmark task against control task) are shown. (B) Same information is shown for the participants with atypical language lateralization. (C) Correlation of the lateralization patterns for all participants is displayed. In all but one participant, language production and spatial attention lateralized to opposite hemispheres regardless of whether the lateralization pattern was typical. Black diamonds show the outcome of the comparison between the Landmark (LM) and LM control (LMC) tasks. The gray triangles show the outcome of the analysis when the laterality index of the Landmark task is based on a comparison between the Landmark task and “rest” conditions, which gives less clear data. SPL, superior parietal lobule.