Redefining the role of Broca’s area in speech

Abstract

For over a century neuroscientists have debated the dynamics by which human cortical language networks allow words to be spoken. Although it is widely accepted that Broca's area in the left inferior frontal gyrus plays an important role in this process, it was not possible, until recently, to detail the timing of its recruitment relative to other language areas, nor how it interacts with these areas during word production. Using direct cortical surface recordings in neurosurgical patients, we studied the evolution of activity in cortical neuronal populations, as well as the Granger causal interactions between them. We found that, during the cued production of words, a temporal cascade of neural activity proceeds from sensory representations of words in temporal cortex to their corresponding articulatory gestures in motor cortex. Broca's area mediates this cascade through reciprocal interactions with temporal and frontal motor regions. Contrary to classic notions of the role of Broca's area in speech, while motor cortex is activated during spoken responses, Broca's area is surprisingly silent. Moreover, when novel strings of articulatory gestures must be produced in response to nonword stimuli, neural activity is enhanced in Broca's area, but not in motor cortex. These unique data provide evidence that Broca's area coordinates the transformation of information across large-scale cortical networks involved in spoken word production. In this role, Broca's area formulates an appropriate articulatory code to be implemented by motor cortex.Broca | speech | ECoG S poken word production is fundamental to human communication. Paul Broca was the first to link word production to a cortical region in the posterior inferior frontal gyrus, since referred to as "Broca's area" (1). His iconic findings are among the most influential in the field of cortical specialization, and Broca's area is still considered to be critically involved in speech production (2, 3).The role of Broca's area in production has been extensively studied using paradigms that vary in complexity from single words to full discourse (4, 5). Although these tasks engage multiple different cognitive demands (e.g., phonological, semantic, and syntactic processing), they all share a common set of core operations consisting of retrieving a word's phonological representation, translating it into an articulatory code, and coordinating the fine motor movements of the vocal articulators (6). However, current neuropsychological and neurolinguistic theories still debate the exact role that Broca's area plays in this set of core operations (7-9). Indefrey and Levelt (4) proposed that Broca's area accesses a phonological word representation that is compiled sequentially into segments of syllables (i.e., syllabification). This segmental representation is then forwarded to motor regions where it is transformed into an articulatory (i.e., phonetic) code. Recent models of speech production (9), as well as the dual-stream model of speech processing (10), do not limit the artic...

Neural correlate of the construction of sentence meaning

“…6-11) and word-level processes (e.g., refs. [12][13][14][15][16][17][18][19][20][21][22][23][24][25][26]. However, the most distinctive feature of human language is its compositionality: the ability to create and understand complex meanings from novel combinations of words structured into phrases and sentences (27).…”

Broca's area: From speech to music

“…Flinker i sar. [32] su otkrili da tokom izgovaranja, vremenske kaskade neuralne aktivnosti napreduju od senzornih reprezentacija reči u temporalnom korteksu do njihovih odgovarajućih artikulatornih pokreta u motornom korteksu. Brokino područje je u ovom slučaju medijator ove kaskade kroz recipročne interakcije sa temporalnim i frontalnim motornim neuronima.…”

“…Suprotno klasičnom shvatanju uloge Bro-kine zone u govoru, dok je motorni korteks aktiviran u toku davanja usmenih odgovora, Brokina zona je iznenađujuće mirna. Tačnije, kada se produkuju novi nizovi artikulatornih pokreta kao odgovor na neverbalni stimulus, neuralna aktivnost se poboljšava u Brokinoj zoni, ali ne i u motornom korteksu [32]. To dokazuje da Brokina oblast koordinira transformacijom informacija kroz široke oblasti kortikalnih mreža koje su uključene u proces govorne produkcije.…”

“…Brokina zona formuliše adekvatan artikulacioni kod koji se ostvaruje motornim korteksom. Iako ovakvi zadaci zahtevaju različite kognitivne procese (fonološke, sintaksičke i semantičke), oni svi dele zajednički set kortikalnih operacija koji se sastoji od preuzimanja fonološke reprezentacije reči, njenog prevođenja u artikulacioni kod, kao i koordinisanje finih motornih pokreta artikulacije [32]. Ipak se i dalje postavlja pitanje o tačnoj ulozi Brokine zone u ovom setu kortikalnih operacija.…”

“…[32] su dokazali da se tokom zadataka na kojima se zahteva produkcija reči, kao što je auditorno ponavljanje reči, neuralne reprezentacije izgovorenih reči prosleđuju od senzornih oblasti do prefrontalnog korteksa, gde Brokina zona povezuje reprezentacije sa artikulatornim kodom koji se zatim sprovodi do motornog korteksa odgovornog za koordinaciju artikulacije. Iako je kod Brokine afazije jedno od najupadljivijih oštećenja deficit motorne produkcije, deluje iznenađujuće da sama Brokina zona nije uključena u proces krajnje artikulacije.…”