More Than Words: Extra-Sylvian Neuroanatomic Networks Support Indirect Speech Act Comprehension and Discourse in Behavioral Variant Frontotemporal Dementia

Abstract

Indirect speech acts—responding “I forgot to wear my watch today” to someone who asked for the time—are ubiquitous in daily conversation, but are understudied in current neurobiological models of language. To comprehend an indirect speech act like this one, listeners must not only decode the lexical-semantic content of the utterance, but also make a pragmatic, bridging inference. This inference allows listeners to derive the speaker’s true, intended meaning—in the above dialog, for example, that the speaker cannot provide the time. In the present work, we address this major gap by asking non-aphasic patients with behavioral variant frontotemporal dementia (bvFTD, n = 21) and brain-damaged controls with amnestic mild cognitive impairment (MCI, n = 17) to judge simple question-answer dialogs of the form: “Do you want some cake for dessert?” “I’m on a very strict diet right now,” and relate the results to structural and diffusion MRI. Accuracy and reaction time results demonstrate that subjects with bvFTD, but not MCI, are selectively impaired in indirect relative to direct speech act comprehension, due in part to their social and executive limitations, and performance is related to caregivers’ judgment of communication efficacy. MRI imaging associates the observed impairment in bvFTD to cortical thinning not only in traditional language-associated regions, but also in fronto-parietal regions implicated in social and executive cerebral networks. Finally, diffusion tensor imaging analyses implicate white matter tracts in both dorsal and ventral projection streams, including superior longitudinal fasciculus, frontal aslant, and uncinate fasciculus. These results have strong implications for updated neurobiological models of language, and emphasize a core, language-mediated social disorder in patients with bvFTD.

The entire brain, more or less, is at work: ‘Language regions’ are artefacts of averaging

“…Many other examples can be provided that non-‘language regions’ are involved in language beyond their role in sensorimotor representations and semantic or conceptual processing. To give a non-exhaustive overview, orbitofrontal cortex, among other regions, plays a role in indirect speech act comprehension (92). The dorsolateral prefrontal cortex (part of the putative MDN) plays numerous specific roles in ‘discourse management, integration of prosody, interpretation of nonliteral meanings, inference making, ambiguity resolution, and error repair’ (93).…”

Language impairment in the genetic forms of behavioural variant frontotemporal dementia

“…People with bvFTD can have difficulties with participating in communication in the first place [ 26 ], as well as how best to communicate effectively [ 25 ]. These deficits are likely to arise from a combination of executive function and social cognition deficits that are present here in each of the three genetic groups [ 27 , 28 ].…”