Causal Contributions of the Domain-General (Multiple Demand) and the Language-Selective Brain Networks to Perceptual and Semantic Challenges in Speech Comprehension

Abstract

Listening to spoken language engages domain-general multiple demand (MD; frontoparietal) regions of the human brain, in addition to domain-selective (frontotemporal) language regions, particularly when comprehension is challenging. However, there is limited evidence that the MD network makes a functional contribution to core aspects of understanding language. In a behavioural study of volunteers (n = 19) with chronic brain lesions, but without aphasia, we assessed the causal role of these networks in perceiving, comprehending, and adapting to spoken sentences made more challenging by acoustic-degradation or lexico-semantic ambiguity. We measured perception of and adaptation to acoustically degraded (noise-vocoded) sentences with a word report task before and after training. Participants with greater damage to MD but not language regions required more vocoder channels to achieve 50% word report, indicating impaired perception. Perception improved following training, reflecting adaptation to acoustic degradation, but adaptation was unrelated to lesion location or extent. Comprehension of spoken sentences with semantically ambiguous words was measured with a sentence coherence judgement task. Accuracy was high and unaffected by lesion location or extent. Adaptation to semantic ambiguity was measured in a subsequent word association task, which showed that availability of lower-frequency meanings of ambiguous words increased following their comprehension (word-meaning priming). Word-meaning priming was reduced for participants with greater damage to language but not MD regions. Language and MD networks make dissociable contributions to challenging speech comprehension: Using recent experience to update word meaning preferences depends on language-selective regions, whereas the domain-general MD network plays a causal role in reporting words from degraded speech.

Keywords: adaptation; language comprehension; learning; lesion; multiple demand (MD) system; semantic ambiguity; speech perception.

Figure 1.

Language and multiple demand (MD) networks, participant lesion maps, and lesion volumes. (A) The language and MD networks against which we compared participants’ lesions. The images show probabilistic activation maps of the language network and the MD network based on fMRI data from large numbers of neurotypical participants (language: n = 220; MD: n = 63), which have been thresholded to show regions active in at least 5% of participants during the relevant functional task and plotted onto a volume rendering of the brain. (B) Volume of lesion falling into each network for each of the 19 participants in the present study. Solid line depicts an equal volume of each network affected by the lesion. Different colours/shapes indicate assignment of the participants into the LANGUAGE (LANG), MD, and OTHER Groups upon which recruitment was based (for categorical group analyses, see Supporting Information). (C) Lesion overlap across participants depicted on volume renderings of the brain and on midline sagittal slices viewed as if from the left or right (Montreal Neurological Institute (MNI) space x coordinates of −8 and +8, cross-hairs show the location of y = 0, z = 0 in these slices). Images are shown separately for participants originally assigned to each of the three groups (see Supporting Information for group analyses). Two participants assigned to the MD group (md6, md10) contributed data to tasks for only one type of challenge and therefore images are shown separately for the two challenge types. Brighter colours reflect greater lesion overlap across participants.

Figure 2.

Word report task results. (A) Word report accuracy scores for different levels of degradation and the pre- and post-training tests separately. Bars show mean values across all 18 participants and error bars show ±1 SEM, adjusted to remove between-subject variance (Morey, 2008). (B) Psychometric logistic function fits separately for the pre-training (solid) and post-training (dashed) data for the mean across all 18 participants (black colour) and each participant separately (coloured by group). The horizontal line indicates the 50% word report accuracy threshold. Vertical lines indicate the estimated threshold number of channels corresponding to the 50% word report accuracy threshold for the mean fits across all 18 participants. (C) Estimated threshold number of channels (log scale) required for 50% accuracy in the word report task for the pre- and post-training tests separately. Bars show mean values across all 18 participants and error bars show ±1 SEM, adjusted to remove between-subject variance (Morey, 2008). Individual participant values are overlaid (colour and shape reflect participant group; see Supporting Information).

Figure 3.

Relationship between speech perception and lesion volume. Individual participant data for estimated threshold number of channels (log scale) required for 50% word report accuracy for the mean of pre- and post-training tests plotted separately against damage to the language network, to the multiple demand (MD) network, and total damage (colour and shape reflect participant group; see Supporting Information). Higher threshold number of channels indicates worse speech perception performance. The dashed line shows the linear best fit, and grey shaded areas show 95% confidence intervals.

Figure 4.

Sentence coherence task results. (A) Proportion of errors and (B) response times measured from sentence offset for coherence judgements to low-ambiguity and high-ambiguity sentences. In each case, bars reflect the mean values across all 18 participants and error bars show ±1 SEM, adjusted to remove between-subject variance (Morey, 2008). Individual participant values are plotted (colour and shape reflect participant group; see Supporting Information).

Figure 5.

Word association task results, showing proportion of responses consistent with the subordinate meaning for ambiguous words in the Unprimed and Primed conditions. Bars reflect the mean values across all 18 participants and error bars show ±SEM, adjusted to remove between-subject variance. Individual participant values are plotted (colour and shape reflect participant group; see Supporting Information).

Figure 6.

Relationship between word meaning priming and lesion volume. Individual participant data for word meaning priming effects estimated from the model residuals, plotted separately against damage to the language network and to the multiple demand (MD) network, and against total damage (colour and shape reflect participant group; see Supporting Information). The dashed line shows the linear best fit, and grey shaded areas show 95% confidence intervals.