Network dynamics of Broca’s area during word selection

Abstract

19 20 ¶ These authors contributed equally to this work. 21 22 23Current models of word-production in Broca's area posit that sequential and staggered semantic, 24 lexical, phonological and articulatory processes precede articulation. Using millisecond-resolution 25 intra-cranial recordings, we evaluated spatiotemporal dynamics and high frequency functional 26 interconnectivity between ventro-lateral prefrontal regions during single-word production. Through 27 the systematic variation of retrieval, selection, and phonological loads, we identified specific 28 activation profiles and functional coupling patterns between these regions that fit within current 29 psycholinguistic theories of word production. However, network interactions underpinning these 30 processes activate in parallel (not sequentially), while the processes themselves are indexed by 31 specific changes in network state. We found evidence that suggests that pars orbitalis is coupled 32 with pars triangularis during lexical retrieval, while lexical selection in Broca's area is terminated via 33 coupled activity with M1 at articulation onset. Taken together, this work reveals that speech 34 production relies on very specific inter-regional couplings in rapid sequence in the language 35 dominant hemisphere. 36 37 slow, and that semantico-lexical, phonological and articulatory processes occur sequentially, with 50 hand-off occurring from the end of one process, to enable the next [17, 18]. However, recent work, 51 suggests that very early (within 200 ms) after input, acoustic structure and semantics are already 52 being processed [13, 19, 20]. Additionally, functional imaging techniques have also been used to 53 ascribe this stepwise ontology of word production to distinct sub-regions of Broca's area, and can 54 parsimoniously be interpreted as implying that linguistic process reside in a distinct cortical 55 region [17, 18,[21][22][23]. 56 57 Over the last decade, invasive recordings of human cortex have led to novel insights into language 58 mechanisms [6,[24][25][26][27]. However, these studies have evaluated the spatial and temporal 59 characteristics of individual regions in isolation, with limited, if any, analyses of the network 60 behavior likely underpinning them [6]. Here, we seek to evaluate how linguistic processes are 61 effected by networks connecting sub-regions involved in these processes, and whether changes in 62 network state index the transition from one constituent process to the next. 63 64To derive this network-based description of dynamics within the IFG during word production, we 65 collected data in a large cohort (n=27) of patients with experimental conditions that varied retrieval, 66 selection, and phonological loads. We specifically evaluated interactions between sub-regions of 67 the IFG and motor cortex in the sub-central gyrus (sCG) during the intervals at which constituent 68 linguistic processes might occur. Intermediary states identified in the functional network connecting 69 the components of the IFG during object ...

A Vector Space Model for Neural Network Functions: Inspirations From Similarities Between the Theory of Connectivity and the Logarithmic Time Course of Word Production

“…Corresponding studies have suggested staged (Indefrey and Levelt, 2004 ) or overlapping (Riès et al, 2017 ; Conner et al, 2019 ) processes of lexical selection, phonological retrieval, and encoding, which mainly involve left lateralized fronto-temporal networks (Indefrey and Levelt, 2000 ; Binder and Desai, 2011 ; Robinson et al, 2012 ; Mirman et al, 2015 ). A recent connectivity analysis identified smooth transitions between an initial state modulating task-directed attention, possibly enabling activation spread, an early stage associated with lexical retrieval, a later stage associated with lexical selection and phonological encoding, and finally articulation, altogether indicating an interactive processing (Conner et al, 2019 ). VF, however, differs from picture naming in some regards, including the production of as many words as possible to only one stimulus and the prohibition of word repetition.…”

“…This seems reminiscent of the activation of multiple concepts, which has been proposed to occur as a prerequisites of item selection (Indefrey and Levelt, 2004 ) in the course of word production. Spatiotemporal dynamics of the respective processes of word production have mainly been characterized for picture naming tasks (e.g., Billingsley et al, 2004 ; Indefrey and Levelt, 2004 ; Riès et al, 2017 ; Conner et al, 2019 ). Corresponding studies have suggested staged (Indefrey and Levelt, 2004 ) or overlapping (Riès et al, 2017 ; Conner et al, 2019 ) processes of lexical selection, phonological retrieval, and encoding, which mainly involve left lateralized fronto-temporal networks (Indefrey and Levelt, 2000 ; Binder and Desai, 2011 ; Robinson et al, 2012 ; Mirman et al, 2015 ).…”

“…Spatiotemporal dynamics of the respective processes of word production have mainly been characterized for picture naming tasks (e.g., Billingsley et al, 2004 ; Indefrey and Levelt, 2004 ; Riès et al, 2017 ; Conner et al, 2019 ). Corresponding studies have suggested staged (Indefrey and Levelt, 2004 ) or overlapping (Riès et al, 2017 ; Conner et al, 2019 ) processes of lexical selection, phonological retrieval, and encoding, which mainly involve left lateralized fronto-temporal networks (Indefrey and Levelt, 2000 ; Binder and Desai, 2011 ; Robinson et al, 2012 ; Mirman et al, 2015 ). A recent connectivity analysis identified smooth transitions between an initial state modulating task-directed attention, possibly enabling activation spread, an early stage associated with lexical retrieval, a later stage associated with lexical selection and phonological encoding, and finally articulation, altogether indicating an interactive processing (Conner et al, 2019 ).…”

“…Despite a vast knowledge gain in recent decades (for a review see Price, 2012 ), the complexity of the systems and processes underlying word production naturally leaves open questions and controversies. There is, however, wide agreement on core processes encompassing conceptual preparation, lexical selection, and form encoding (e.g., Dell, 1986 ; Levelt, 1999 ; Indefrey and Levelt, 2004 ; for a review see Henry and Crawford, 2005 ; Walker and Hickok, 2016 ) which especially involve the activation of left lateralized frontotemporal cortical networks (Indefrey and Levelt, 2000 ; Binder and Desai, 2011 ; Robinson et al, 2012 ; Mirman et al, 2015 ; Conner et al, 2019 ). Moreover, a wide-spread cortical system (Indefrey and Levelt, 2000 ; Riès et al, 2017 ) seems to be involved in the initial activation of semantic concepts, i.e., non-verbal representations of an object's sensory, motor, and affective features (encompassing, e.g., shape, use, familiarity, and relationships with other objects; Levelt, 1999 ; Pulvermüller, 1999 ; Binder and Desai, 2011 ; Kiefer and Pulvermüller, 2012 ; Rofes et al, 2019 ).…”

Minimal phrase composition revealed by intracranial recordings

“…The portion of temporal pole and MTG exhibiting alpha increases during the anticipatory window could be also involved in late-stage lexicoconceptual processing of adjectival representations, although given the relatively late postadjective window it is more likely to be related to anticipation. Relatedly, given increasing evidence for IFG involvement in linear morpho-syntactic processing and complex sentential syntax (Matchin and Hickok, 2020), as opposed to elementary syntactic structure building, it is also possible that the beta effect in pars triangularis indexes a form of lexical anticipation (for word frequency effects in pars triangularis via functional coupling with subcentral gyrus, see Conner et al 2019), with strictly syntactic anticipation being localized to temporal pole and MTG. A recent review of event-related potentials implicated in processing predictable words (the N400) also specifically pinpointed anterior IFG and LATL in preceding cortical activations (Pulvermüller and Grisoni, 2020), mapping onto the present results.…”