A core speech circuit between primary motor, somatosensory, and auditory cortex: evidence from connectivity and genetic descriptions

Abstract

What adaptations allow humans to produce and perceive speech so effortlessly? We show that speech is supported by a largely undocumented core of structural and functional connectivity between the central sulcus (CS or primary motor and somatosensory cortex) and the transverse temporal gyrus (TTG or primary auditory cortex). Anatomically, we show that CS and TTG cortical thickness covary across individuals and that they are connected by white matter tracts. Neuroimaging network analyses confirm the functional relevance and specificity of these structural relationships. Specifically, the CS and TTG are functionally connected at rest, during natural audiovisual speech perception, and are coactive over a large variety of linguistic stimuli and tasks. Importantly, across structural and functional analyses, connectivity of regions immediately adjacent to the TTG are with premotor and prefrontal regions rather than the CS. Finally, we show that this structural/functional CS-TTG relationship is mediated by a constellation of genes associated with vocal learning and disorders of efference copy. We propose that this core circuit constitutes an interface for rapidly exchanging articulatory and acoustic information and discuss implications for current models of speech.

Neural source dynamics of brain responses to continuous stimuli: speech processing from acoustics to comprehension

“…Motor cortex involvement in speech perception is predicted by the motor theory of speech perception (see Galantucci, Fowler, & Turvey, 2006) and has been demonstrated with meaningless syllables and single word stimuli (Pulvermüller et al, 2006;Schomers, Kirilina, Weigand, Bajbouj, & Pulvermüller, 2015;Wilson, Saygin, Sereno, & Iacoboni, 2004). Recent evidence suggests that this functional integration is supported by tight anatomical connections between Heschl's gyrus and primary motor and somatosensory cortex (Skipper & Hasson, 2017). Our result of rapid bilateral responses is compatible with a bilateral mechanism for a unified sensory-motor representation of speech (Cogan et al, 2014).…”

“…Motor cortex involvement in speech perception is predicted by the motor theory of speech perception (see Galantucci, Fowler, & Turvey, 2006) and has been demonstrated with meaningless syllables and single word stimuli (Pulvermüller et al, 2006;Schomers, Kirilina, Weigand, Bajbouj, & Pulvermüller, 2015;Wilson, Saygin, Sereno, & Iacoboni, 2004). Recent evidence suggests that this functional integration is supported by tight anatomical connections between Heschl's gyrus and primary motor and somatosensory cortex (Skipper & Hasson, 2017). The left posterior IFG is thought to be part of the dorsal stream of speech processing, involved in mapping between acoustic and motor representations (Hickok & Poeppel, 2004;Saur et al, 2008), although evidence from neurological patients suggests that it is not necessary for speech comprehension (Rogalsky, Love, Driscoll, Anderson, & Hickok, 2011).…”

Prominence of delta oscillatory rhythms in the motor cortex and their relevance for auditory and speech perception

“…While the evidence we have considered indicates that the motor cortex is a constitutive part of the 'auditory system', the mechanisms and pathways controlling the gain of auditory processing and perception is currently unclear. In particular, while the primary motor, somatosensory, and auditory cortex seem to be strongly interconnected (Skipper and Hasson 2017), evidence of direct projections between motor and auditory regions in humans is currently lacking (Morillon et al 2015). Importantly, multiple neural structures related to motor or attentional (Fiebelkorn et al 2018;Wyart et al 2012) processes temporally constrain sensory processing.…”

A Modulatory Effect of Brief Passive Exposure to Non-linguistic Sounds on Intrinsic Functional Connectivity: Relevance to Cognitive Performance

“…In addition to the increased auditory-attention iFC in the AG, both L.HG and R.HG connections with the precentral gyrus, the site of the premotor cortex, were increased in the CG only. Given that this auditory-motor circuitry is strong during rest and speech perception ( Skipper and Hasson 2017 ), individuals in the CG may have been more greatly involved in inner speech ( Bastian et al 2017 ) or spontaneous thoughts ( Chou et al 2017 ) while “mind-wandering” at rest, relative to those in the AG whose mind wandering was potentially disrupted during or at the beginning of the auditory exposure. This assumption needs to be tested by linking iFC to resting-state cognition (e.g., the presence/frequency of mind wandering), assessed by post-MRI questionnaires ( Delamillieure et al 2010 ; Diaz et al 2013 ).…”