Dissociated repetition deficits in aphasia can reflect flexible interactions between left dorsal and ventral streams and gender-dimorphic architecture of the right dorsal stream

Abstract

Assessment of brain-damaged subjects presenting with dissociated repetition deficits after selective injury to either the left dorsal or ventral auditory pathways can provide further insight on their respective roles in verbal repetition. We evaluated repetition performance and its neural correlates using multimodal imaging (anatomical MRI, DTI, fMRI, and(18)FDG-PET) in a female patient with transcortical motor aphasia (TCMA) and in a male patient with conduction aphasia (CA) who had small contiguous but non-overlapping left perisylvian infarctions. Repetition in the TCMA patient was fully preserved except for a mild impairment in nonwords and digits, whereas the CA patient had impaired repetition of nonwords, digits and word triplet lists. Sentence repetition was impaired, but he repeated novel sentences significantly better than clichés. The TCMA patient had tissue damage and reduced metabolism in the left sensorimotor cortex and insula. DTI showed damage to the left temporo-frontal and parieto-frontal segments of the arcuate fasciculus (AF) and part of the left ventral stream together with well-developed right dorsal and ventral streams, as has been reported in more than one-third of females. The CA patient had tissue damage and reduced metabolic activity in the left temporoparietal cortex with additional metabolic decrements in the left frontal lobe. DTI showed damage to the left temporo-parietal and temporo-frontal segments of the AF, but the ventral stream was spared. The direct segment of the AF in the right hemisphere was also absent with only vestigial remains of the other dorsal subcomponents present, as is often found in males. fMRI during word and nonword repetition revealed bilateral perisylvian activation in the TCMA patient suggesting recruitment of spared segments of the left dorsal stream and right dorsal stream with propagation of signals to temporal lobe structures suggesting a compensatory reallocation of resources via the ventral streams. The CA patient showed a greater activation of these cortical areas than the TCMA patient, but these changes did not result in normal performance. Repetition of word triplet lists activated bilateral perisylvian cortices in both patients, but activation in the CA patient with very poor performance was restricted to small frontal and posterior temporal foci bilaterally. These findings suggest that dissociated repetition deficits in our cases are probably reliant on flexible interactions between left dorsal stream (spared segments, short tracts remains) and left ventral stream and on gender-dimorphic architecture of the right dorsal stream.

Keywords: conduction aphasia; diffusion tensor tractography; dual dorsal-ventral pathways; functional magnetic resonance imaging; positron emission tomography; repetition; transcortical motor aphasia.

Figure 1

Lichtheim's first diagram of speech centers, commissural pathways and predicted sites of lesions that would cause aphasia (left image). In this diagram, “A” indicates the center of auditory images, “M” the center of motor images, and “B” the center of concepts. Lesions interrupting the commissure “A”-“M” cause conduction aphasia (CA) (red line), whereas interruption of the commissure interconnecting B-M causes transcortical motor aphasia (TCMA) (yellow line). Diagram depicting a two route model to repetition (right image) (adapted from McCarthy and Warrington, 1984). The green circle represents the route that should be interrupted to induce CA, whereas the purple circle represents a lesion in the connection that should be interrupted to induce TCMA.

Figure 2

Left hemisphere structural lesions. Axial T₁-weighted MRI showing a small infarction in the patient with transcortical motor aphasia (A) involving the left sensorimotor cortex and medial insula (white arrows). The lesion is superficial sparing the deep white matter. The MRI in the patient with conduction aphasia shows a small infarction involving the left posterior temporal gyrus and supramarginal gyrus extending deeply into the lateral ventricle wall (B) (white arrows). The left hemisphere is represented on the left side of the images. DTI, MRI, and PET of the corpus callosum. Brain imaging of the corpus callosum. Midsaggital DTI (C) and ¹⁸FDG-PET images (D) and coronal T₁-weighted MRI (E) of the corpus callosum in patients RTP (top panel) and JGG (bottom panel). In RPT the corpus callosum was structurally (C) and functionally intact (D). Although RTP had an infarction in the left sensorimotor cortex, this did not result in noticeable changes in the anterior segments of the corpus callosum. The rostral body of corpus callosum in JGG shows diminished streamlines (C), bottom panel (yellow arrowheads) and decrement of metabolic activity (D), bottom panel (yellow arrow). The fact that structural and functional involvement of the anterior corpus callosum in JGG does not interrupt fibers interconnecting the damaged left temporoparietal cortex with its homologous in the right hemisphere suggests that corpus callosum involvement was unrelated to the stroke lesion. Anatomical MRIs show normal septum pellucidum (grade 0, normal) (yellow arrow) in RTP (E), top panel and an enlarged cavum septum pellucidum (grade 4, severe) (Degreef et al., ; DeLisi et al., ; Kim and Peterson, 2003) in JGG (yellow arrows) (E, bottom panel).

Figure 3

Uninflated surface of the right (A) and left hemispheres (B) (FreeSurfer reconstruction) of the patient with transcortical motor aphasia (RTP) showing gyri cultured in green with sulci shown in red. DTI of right hemisphere perisylvian pathways superimposed on RTP anatomical MRI shows well-developed temporo-frontal, temporo-parietal and parieto-frontal streams (red, yellow, and purple, respectively) and ventral stream (blue) (A), whereas in the left hemisphere only the parieto-temporal segment of the arcuate fasciculus (yellow) and part of the ventral stream (blue) could be reconstructed (B). This image also shows the location of the infarct in the lower pericentral region (red area). Parasaggital T₁-weighted MRI view of the left hemisphere shows the infarction in the sensorimotor cortex (white arrows) and medial insula (yellow arrow) (C). Parasaggital view of the ¹⁸FDG-PET (MRIcroN) showing an area of reduced metabolic activity in the left fronto-insular region (blue) (D) which is slightly larger than the area of infarction depicted in (C). See further details in Table 4.

Figure 4

DTI, MRI, and PET. Uninflated surface of the right (A) and left hemispheres (B) (FreeSurfer reconstruction) of the patient with conduction aphasia (JGG) showing gyri cultured in green with sulci shown in red. DTI of right hemisphere perisylvian pathways superimposed on JJG anatomical MRI shows a complete lack of the direct temporo-frontal section of the AF in the right hemisphere. The indirect temporo-parietal (yellow) and parieto-frontal (purple) segments are present but very small. White matter tract reconstruction in the left hemisphere shows that the fronto-parietal segment of the AF (purple) was intact, but the temporo-parietal and temporo-frontal segments were unreconstructable, and seemingly destroyed by the lesion (B). The ventral stream (inferior frontal-occipital fasciculus/extreme capsule) was reconstructed successfully in both hemispheres (A,B). The surface image of the left hemisphere depicted in (B) also shows the infarction (red area) involving the posterior-superior and middle temporal gyri and part of the supramarginal gyrus. Parasaggital T₁-weighted image shows a component of the infarction in the supramarginal gyrus (white arrow) surrounded by perinecrotic tissue (yellow arrow) (C). Parasaggital image of the ¹⁸FDG-PET (MRIcroN) showing an area of reduced metabolic activity in the left temporoparietal region (red) (D) which is slightly larger at the level of the posterior temporal gyrus than the area of infarction depicted in (C). Less voluminous foci of reduced metabolic activity (all in red) are also shown in the left middle frontal gyrus (Brodmann's area 6), lateral orbitofrontal cortex (Brodmann's area 11), inferior temporal gyrus (Brodmann's area 20), and cerebellum (D). See further details in Table 4.

Figure 5

Functional MRI. The figures show the contrast words (A), nonwords (B), and word triplets (C) versus rest. Contrasts are shown on patients' uninflated cortical surface of the right and left hemispheres and significant activations (p < 0.05, corrected) are depicted in light blue and blue. The fMRI shows bilateral perisylvian activation in both patients in all three tasks. Although JGG obtained lower performance in word and nonword repetition tasks than RTP, he showed greater areas of activation, extending into motor, premotor and prefrontal areas in addition to the perisylvian areas activated by both of them. In contrast, word triplet repetition activated a greater bilateral network in RTP than JGG. See further details in text and Table 3.

Figure 6

¹⁸FDG-PET. Axial PET images (MRIcroN) of patients with transcortical motor aphasia (blue) and conduction aphasia (red) showing significant reductions of metabolic activity in the left perisylvian areas and interconnected areas (see Table 4). Note that although the structural lesion in RTP was more superficial than the one in JGG (see Figure 2), decreased metabolic activity extended deeply to affect white matter in both cases. The left hemisphere is represented on the left side of the images.