Reductions in prefrontal activation predict off-topic utterances during speech production

Paul Hoffman

doi:10.1038/s41467-019-08519-0

Abstract

The ability to speak coherently is essential for effective communication but declines with age: older people more frequently produce tangential, off-topic speech. Little is known, however, about the neural systems that support coherence in speech production. Here, fMRI was used to investigate extended speech production in healthy older adults. Computational linguistic analyses were used to quantify the coherence of utterances produced in the scanner, allowing identification of the neural correlates of coherence for the first time. Highly coherent speech production was associated with increased activity in bilateral inferior prefrontal cortex (BA45), an area implicated in selection of task-relevant knowledge from semantic memory, and in bilateral rostrolateral prefrontal cortex (BA10), implicated more generally in planning of complex goal-directed behaviours. These findings demonstrate that neural activity during spontaneous speech production can be predicted from formal analysis of speech content, and that multiple prefrontal systems contribute to coherence in speech.

Highlights

The ability to speak coherently is essential for effective communication but declines with age: older people more frequently produce tangential, off-topic speech
Collection of fMRI data during extended speech production has sometimes been considered problematic due to signal contamination caused by excessive head and jaw movements[13]
A small number of neuroimaging studies have overcome these technical challenges,. These indicate that, in addition to engaging areas involved in motor planning and production, extended speech production activates an left-lateralised network including ventral temporal and inferior parietal regions involved in the representation of semantic knowledge and prefrontal regions associated with planning and cognitive control[14,15,16,17,18]

Summary

Introduction

The ability to speak coherently is essential for effective communication but declines with age: older people more frequently produce tangential, off-topic speech. Older adults are more likely to produce tangential, off-topic utterances during conversation[3,4] and to provide irrelevant information when telling a story[2] or describing an object[5] These effects have been observed in a range of tasks, age-related coherence declines are most pronounced when individuals provide information from their own memory or personal experience, and less severe when they describe visually presented stimuli, such as pictures or comic strips[1,6,7]. One view is that declines in coherence result from a reduced ability to inhibit irrelevant information, which means that older people are less able to prevent tangential or off-topic ideas from intruding into their discourse[4,11] Supporting this idea, a recent behavioural study demonstrated that the ability to select task-relevant aspects of semantic knowledge is a strong determinant of coherence[12]. The majority of participants in these studies were healthy young adults, ; no studies to date have used fMRI to investigate extended speech production in older people

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