Re-examining the brain regions crucial for orchestrating speech articulation

Abstract

A traditional method of localizing brain functions has been to identify shared areas of brain damage in individuals who have a particular deficit. The rationale of this 'lesion overlap' approach is straightforward: if the individuals can no longer perform the function, the area of brain damaged in most of these individuals must have been responsible for that function. However, the reciprocal association, i.e. the probability of the lesion causing the deficit, is often not evaluated. In this study, we illustrate potential weaknesses of this approach, by re-examining regions of the brain essential for orchestrating speech articulation. A particularly elegant and widely cited lesion overlap study identified the superior part of the precentral gyrus of the insula (in the anterior insula) as the shared area of damage in chronic stroke patients with 'apraxia of speech', a disorder of motor planning and programming of speech. Others have confirmed that patients with apraxia of speech commonly have damage to the anterior insula. However, this reliable association might reflect the vulnerability of the insula to damage following occlusion or narrowing of the middle cerebral artery (which can independently cause apraxia of speech and many other deficits). To evaluate this possibility, we examined the relationship between apraxia of speech and the insula in three unique ways: (i) we determined the probability of the lesion causing the deficit, as well as the deficit being associated with the lesion, by examining speech articulation and advanced MRIs in two consecutive series of patients with acute left hemisphere, non-lacunar stroke, 40 with and 40 without insular damage; (ii) we studied patients at stroke onset to identify the deficit before it resolved in cases of small stroke; and (iii) we identified regions of dysfunctional brain tissue, as well as structural damage. Using this approach, we found no association between apraxia of speech and lesions of the left insula, anterior insula or superior tip of the precentral gyrus of the insula. Instead, in patients with and without insular lesions, apraxia of speech was associated with structural damage or low blood flow in left posterior inferior frontal gyrus. These results illustrate a potential limitation of lesion overlap studies, and illustrate an alternative method for identifying brain-behaviour relationships.

Neural mechanisms underlying auditory feedback control of speech

“…Wise et al, 1999;Bohland and Guenther, 2006;Ozdemir et al, 2006;Soros et al, 2006). These findings appear to conflict with the large body of lesion data that supports the traditional view of left hemisphere dominance of speech production (Duffy, 1995;Dronkers, 1996;Kent and Tjaden, 1997;Hillis et al, 2004). The present results reconcile these findings: while both hemispheres contribute to speech production, feedforward control is predominantly subserved by the left hemisphere whereas auditory feedback control is subserved by right hemisphere frontal regions.…”

Nasal consonant production in Broca’s and Wernicke’s aphasics: Speech deficits and neuroanatomical correlates

“…Recent lesion studies (Dronkers, 1996;Bates et al, 2003;Dronkers, Ogar, Willock, and Wilkins, 2004) as well as functional neuroimaging studies (Wise et al, 1999;Ackermann andRiecker, 2004,Shuster andLemieux, 2005) have identified the anterior insula as a critical area subserving articulatory planning or implementation of speech. However, Hillis et al (2004) using diffusion-weighted and perfusion-weighted imaging found no association between apraxia of speech and the left insula but strongly implicated Broca's area in apraxia of speech. The results of the current study do suggest that the insula plays an important role in the coordination of articulatory movements.…”

“…Previous studies implicate anterior brain structures including Broca's area, the pre-motor and motor regions for face and mouth areas, the white matter deep to these structures, the basal ganglia, and the insula (Hillis et al, 2004;Damasio, 1998;Cummings, 1993;Naeser et al, 1989). Moreover, Naeser et al showed increased severity of speech deficit when two neuroanatomical areas were affected by lesion: (1) the most medial and rostral portion of the subcallosal fasciculus (deep to Broca's area) and (2) the periventricular white matter near the body of the lateral ventricle deep to the lower motor/ sensory cortex for mouth (affecting motor execution and feedback).…”

“…That is, the presence of a lesion in an area does not indicate the extent of the damage to an area, a factor which is essential in delineating the functional role a particular neural area may play (cf. Dronkers, 1996; for discussion see Hillis et al, 2004).…”

Thresholding lesion overlap difference maps: Application to category-related naming and recognition deficits

“…For example, since the insula is in the core of the middle cerebral artery territory, insular damage commonly correlates with damage in adjacent locations, and the damage may be co-attributed to the insula by these methods (Hillis et al, 2004).…”