Hippocampus plays a role in speech feedback processing

Vincent Van De Ven,Lourens Waldorp,Ingrid Christoffels

doi:10.1016/j.neuroimage.2020.117319

Vincent Van De Ven, Lourens Waldorp + Show 1 more

Open Access

https://doi.org/10.1016/j.neuroimage.2020.117319

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Journal: NeuroImage	Publication Date: Aug 31, 2020
Citations: 10	License type: cc-by

Affiliation: Maastricht University, University of Amsterdam

Abstract

There is increasing evidence that the hippocampus is involved in language production and verbal communication, although little is known about its possible role. According to one view, hippocampus contributes semantic memory to spoken language. Alternatively, hippocampus is involved in the processing the (mis)match between expected sensory consequences of speaking and the perceived speech feedback. In the current study, we re-analysed functional magnetic resonance (fMRI) data of two overt picture-naming studies to test whether hippocampus is involved in speech production and, if so, whether the results can distinguish between a “pure memory” versus a “prediction” account of hippocampal involvement. In both studies, participants overtly named pictures during scanning while hearing their own speech feedback unimpededly or impaired by a superimposed noise mask. Results showed decreased hippocampal activity when speech feedback was impaired, compared to when feedback was unimpeded. Further, we found increased functional coupling between auditory cortex and hippocampus during unimpeded speech feedback, compared to impaired feedback. Finally, we found significant functional coupling between a hippocampal/supplementary motor area (SMA) interaction term and auditory cortex, anterior cingulate cortex and cerebellum during overt picture naming, but not during listening to one's own pre-recorded voice. These findings indicate that hippocampus plays a role in speech production that is in accordance with a “prediction” view of hippocampal functioning.

Highlights

Language has been viewed as a fronto-temporal neocortical function and studied in isolation from memory
From the perspective of the “expectation” view of hippocampal function, impaired speech feedback will alter hippocampal activity, as the hippocampus is actively involved in processing the degree of mismatch between perceived feedback to sensory expectations derived from memory (Kumaran and Maguire, 2009; de Lange et al, 2018)
We re-analysed the combined fMRI data collected during overt speech production of two studies and found evidence that human hippocampus is involved in monitoring of speech feedback

Summary

Introduction

Language has been viewed as a fronto-temporal neocortical function and studied in isolation from memory. There is growing evidence that the medial temporal lobe (MTL), the hippocampus, contributes to speech production and verbal communication (Duff et al, 2008; Duff and Brown-Schmidt, 2012; Covington and Duff, 2016; Llorens et al, 2016; Piai et al, 2016; Kepinska et al, 2018) One interpretation of this evidence is that verbal communication bears on declarative memory processes that are governed by the hippocampus (Squire and Zola, 1998; Manns et al, 2003; Klooster and Duff, 2015). Adopting a “pure memory” view of hippocampal function one would predict no alternation of hippocampal activity with mismatching speech feedback, as the hippocampus contributed semantic or associative memory content to the speech formation but is not involved in monitoring speech consequences. We tested the involvement of the hippocampus in speech monitoring by analysing whether hippocampal activity and connectivity with areas of the speech monitoring network changes with changing speech feedback quality

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