Neural correlates of differential finger gesture imitation deficits in left hemisphere stroke

Abstract

Behavioural studies in apraxic patients revealed dissociations between the processing of meaningful (MF) and meaningless (ML) gestures. Consequently, the existence of two differential neural mechanisms for the imitation of either gesture type has been postulated. While the indirect (semantic) route exclusively enables the imitation of MF gestures, the direct route can be used for the imitation of any gesture type, irrespective of meaning, and thus especially for ML gestures. Concerning neural correlates, it is debated which of the visuo-motor streams (i.e., the ventral steam, the ventro-dorsal stream, or the dorso-dorsal stream) supports the postulated indirect and direct imitation routes. To probe the hypotheses that regions of the dorso-dorsal stream are involved differentially in the imitation of ML gestures and that regions of the ventro-dorsal stream are involved differentially in the imitation of MF gestures, we analysed behavioural (imitation of MF and ML finger gestures) and lesion data of 293 patients with a left hemisphere (LH) stroke. Confirming previous work, the current sample of LH stroke patients imitated MF finger gestures better than ML finger gestures. The analysis using voxel-based lesion symptom mapping (VLSM) revealed that LH damage to dorso-dorsal stream areas was associated with an impaired imitation of ML finger gestures, whereas damage to ventro-dorsal regions was associated with a deficient imitation of MF finger gestures. Accordingly, the analyses of the imitation of visually uniform and thus highly comparable MF and ML finger gestures support the dual-route model for gesture imitation at the behavioural and lesion level in a substantial patient sample. Furthermore, the data show that the direct route for ML finger gesture imitation depends on the dorso-dorsal visuo-motor stream while the indirect route for MF finger gesture imitation is related to regions of the ventro-dorsal visuo-motor stream.

Fig. 1

Behavioural results. Assessment of the interaction of MEANING by IMITATION DEFICIT (F (1, 291) = 79.14, p < .001): the difference in imitation performance between patients with (n = 61) and without (n = 232) imitation deficit was significant for both MF (mean imitation score ± SD.: patients without imitation deficit: 1.94 ± 0.14; patients with imitation deficit: 1.82 ± 0.31; t (291) = 10.57, p < .001) and ML gesture imitation (mean imitation score ± SD.: patients without imitation deficit: 1.62 ± 0.39; patients with imitation deficit: 0.94 ± 0.53; t (291) = 16.87, p < .001). However, the difference between patients with and without imitation deficits was significantly larger for ML (ΔML, mean difference ± S.E.M. difference: 0.68 ± 0.09) compared to MF (ΔMF, mean difference ± S.E.M. difference: 0.12 ± 0.02, t (291) = 8.90, p < .001) gestures.

Fig. 2

Lesion overlay. Lesion overlay plot for all 293 LH stroke patients where at least 10% (n = 29) of the patients had a lesion, i.e. displayed are only those voxels which were subjected to the VLSM.

Fig. 3

VLSM analysis results. a) Results of the VLSM analysis for the overall finger imitation scores. VLSM-parameter: minimum lesion overlay 10% (n = 29), level of significance p < .05, uncorrected. Please note: this analysis did not reveal any significant voxels at p < .05 after controlling for multiple comparisons using FDR-correction. Thus, in all analyses on finger imitation, results are reported at the uncorrected significance level of p < .05. b) Results of the separate VLSM for the mean imitation scores of a) the three meaningful (MF, red) and the two meaningless (ML, blue) gestures. Magenta voxels represent the overlap between both VLSM (VLSM-parameter: see Fig. 2a). c) Results of the VLSM for the difference between the mean imitation scores of ML minus MF finger gesture imitation (VLSM-parameter: see Fig. 2a). Note that there were no voxels associated with the difference MF minus ML finger imitation at the significance level of p < .05, uncorrected.

Supplementary Fig. 1

Results of the VLSM analysis for hand imitation scores. Note that only 291 of the 293 patients, of whom finger imitation data are reported in the main article, were included in this analysis, since hand imitation scores of two patients were not available. VLSM-parameter: minimum lesion overlay 10% (n = 29), level of significance p < 0.01, FDR-corrected for multiple comparisons.