Abstract

Transcranial magnetic stimulation focused on either the left anterior supramarginal gyrus or opercular part of the left inferior frontal gyrus has been reported to transiently impair the ability to perform phonological more than semantic tasks. Here we tested whether phonological processing abilities were also impaired following lesions to these regions in right-handed, English speaking adults, who were investigated at least 1 year after a left-hemisphere stroke. When our regions of interest were limited to 0.5 cm3 of grey matter centred around sites that had been identified with transcranial magnetic stimulation-based functional localization, phonological impairments were observed in 74% (40/54) of patients with damage to the regions and 21% (21/100) of patients sparing these regions. This classification accuracy was better than that observed when using regions of interest centred on activation sites in previous functional magnetic resonance imaging studies of phonological processing, or transcranial magnetic stimulation sites that did not use functional localization. New regions of interest were generated by redefining the borders of each of the transcranial magnetic stimulation sites to include areas that were consistently damaged in the patients with phonological impairments. This increased the incidence of phonological impairments in the presence of damage to 85% (46/54) and also reduced the incidence of phonological impairments in the absence of damage to 15% (15/100). The difference in phonological processing abilities between those with and without damage to these 'transcranial magnetic stimulation-guided' regions remained highly significant even after controlling for the effect of lesion size. The classification accuracy of the transcranial magnetic stimulation-guided regions was validated in a second sample of 108 patients and found to be better than that for (i) functional magnetic resonance imaging-guided regions; (ii) a region identified from an unguided lesion overlap map; and (iii) a region identified from voxel-based lesion-symptom mapping. Finally, consistent with prior findings from functional imaging and transcranial magnetic stimulation in healthy participants, we show how damage to our transcranial magnetic stimulation-guided regions affected performance on phonologically more than semantically demanding tasks. The observation that phonological processing abilities were impaired years after the stroke, suggests that other brain regions were not able to fully compensate for the contribution that the transcranial magnetic stimulation-guided regions make to language tasks. More generally, our novel transcranial magnetic stimulation-guided lesion-deficit mapping approach shows how non-invasive stimulation of the healthy brain can be used to guide the identification of regions where brain damage is likely to cause persistent behavioural effects.

Highlights

  • Previous research has shown that repetitive transcranial magnetic stimulation (TMS) over either the left supramarginal gyrus (SMG) (Hartwigsen et al, 2010a; Sliwinska et al, 2015) or pars opercularis of the left inferior frontal gyrus (Gough et al, 2005; Hartwigsen et al, 2010b) causes significant slowing in response times when healthy volunteers perform tasks requiring phonological processing relative to tasks requiring semantic processing

  • The TMS sites reported by Hartwigsen et al (2010a, b) without functional localization (À47, 6, 21 for pOp and À45, À39, 45 for SMG) are almost identical to those reported in the functional MRI study by Devlin et al (2003)

  • When we considered the effect of each lesion site separately, we found that the incidence of phonological impairments after damage to (SMG and pOp), (SMG not pOp), and was: 89% (17/19), 90% (9/10) and 80% (20/25), respectively

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Summary

Introduction

Previous research has shown that repetitive transcranial magnetic stimulation (TMS) over either the left supramarginal gyrus (SMG) (Hartwigsen et al, 2010a; Sliwinska et al, 2015) or pars opercularis of the left inferior frontal gyrus (pOp) (Gough et al, 2005; Hartwigsen et al, 2010b) causes significant slowing in response times when healthy volunteers perform tasks requiring phonological processing (e.g. do two words sound the same?) relative to tasks requiring semantic processing (e.g. do two words mean the same?) These TMS findings are consistent with a wealth of functional imaging studies that have shown activation in SMG and/or pOp for phonological relative to semantic tasks (Price et al, 1997; Poldrack et al, 1999; Booth et al, 2002; Devlin et al, 2003; McDermott et al, 2003; Seghier et al, 2004; Gitelman et al, 2005; Simard et al, 2013). The TMS sites reported by Hartwigsen et al (2010a, b) without functional localization (À47, 6, 21 for pOp and À45, À39, 45 for SMG) are almost identical to those reported in the functional MRI study by Devlin et al (2003)

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