Reorganization of the neurobiology of language after sentence overlearning

Abstract

There is a widespread assumption that there are a static set of ‘language regions’ in the brain. Yet, people still regularly produce familiar ‘formulaic’ expressions when those regions are severely damaged. This suggests that the neurobiology of language varies with the extent of word sequence learning and might not be fixed. We test the hypothesis that perceiving sentences is mostly supported by sensorimotor regions involved in speech production and not ‘language regions’ after overlearning. Twelve participants underwent two sessions of behavioural testing and functional magnetic resonance imaging (fMRI), separated by 15 days. During this period, they repeated two sentences 30 times each, twice a day. In both fMRI sessions, participants ‘passively’ listened to those two sentences and novel sentences. Lastly, they spoke novel sentences. Behavioural results confirm that participants overlearned sentences. Correspondingly, there was an increase or recruitment of sensorimotor regions involved in sentence production and a reduction in activity or inactivity for overlearned sentences in regions involved in listening to novel sentences. The global network organization of the brain changed by ∼45%, mostly through lost connectivity. Thus, there was a profound reorganization of the neurobiology of speech perception after overlearning towards sensorimotor regions not considered in most contemporary models and away from the ‘language regions’ posited by those models. These same sensorimotor regions are generally preserved in aphasia and Alzheimer’s disease, perhaps explaining residual abilities with formulaic language. These and other results warrant reconsidering static neurobiological models of language.

Quantitative MRI reveals differences in striatal myelin in children with DLD

“…The dorsal striatum has been implicated in learning through practice, particularly habit formation ( Skipper et al, 2020 ; Yin and Knowlton, 2006 ). A number of groups, including us, have hypothesised that the striatum is a brain region where we might expect to see neural differences in children with DLD ( Krishnan et al, 2016 ; Ullman et al, 2020 ; Ullman and Pierpont, 2005 ).…”

“…In accordance, a series of behavioural studies has suggested that sequential learning in the linguistic and non-linguistic domains is affected in children with DLD ( Hsu and Bishop, 2014 ; Lum et al, 2014 ; but see West et al, 2018 ; West et al, 2021 ). In studies that probe complex sequential production in the vocal domain, the dorsal striatum is implicated ( Rauschecker et al, 2008 ; Simmonds et al, 2014 ; Skipper et al, 2020 ). The striatum is structurally and functionally connected to regions associated with language production, with the head of the dorsolateral caudate nucleus receiving inputs from inferior frontal cortex, and the putamen receiving inputs from motor, premotor, and supplementary motor cortex ( Alexander et al, 1986 ; Jarbo and Verstynen, 2015 ; Lima et al, 2016 ).…”

Quantitative MRI reveals differences in striatal myelin in children with DLD

“…In accordance, a series of behavioural studies has suggested that sequential learning in the linguistic and non-linguistic domains is affected in children with DLD (Hsu & Bishop, 2014;Lum et al, 2014; but see West et al, 2018West et al, , 2021. In studies that probe complex sequential production in the vocal domain, the dorsal striatum is implicated (Rauschecker et al, 2008;Simmonds et al, 2014;Skipper et al, 2020). The striatum is structurally and functionally connected to regions associated with language production, with the head of the dorsolateral caudate nucleus receiving inputs from inferior frontal cortex, and the putamen receiving inputs from motor, premotor and supplementary motor cortex (Alexander et al, 1986;Jarbo & Verstynen, 2015;Lima et al, 2016).…”

“…The dorsal striatum is important for habitual and sequential learning (Graybiel & Grafton, 2015;Yin & Knowlton, 2006), and we hypothesise that it may play an important role in the acquisition of language because of the complexity of sequencing required for language. Indeed, in studies that probe complex sequential production in the vocal domain, the dorsal striatum is implicated (Rauschecker et al, 2008;Simmonds et al, 2014;Skipper et al, 2020). Additionally, a series of behavioural studies has suggested that sequential learning in the linguistic and non-linguistic domains is affected in children with DLD (Hsu & Bishop, 2014;Lum et al, 2014; but see West et al, 2018West et al, , 2021.…”

“…The dorsal striatum has been implicated in learning through practice, particularly habit formation (Skipper et al, 2020;Yin & Knowlton, 2006). A number of groups, including us, have hypothesised that the striatum is a brain region where we might expect to see neural differences in children with DLD (Krishnan et al, 2016;Ullman et al, 2020;Ullman & Pierpont, 2005).…”