Revealing the co-existence of written and spoken language coding neural populations in the left-ventral occipitotemporal cortex

Abstract

Reading relies on the ability to map written symbols with speech sounds. The left ventral occipitotemporal cortex (left-vOT) plays a crucial role in this process. Through the automatization of the mapping ability, this specific part of the ventral visual pathway (a.k.a., the Visual Word Form Area) progressively becomes specialized in written word recognition. Yet, despite its key role in reading, the area also responds to speech. This observation raises questions about the actual nature of neural representations encoded in the left-vOT and, therefore, the underlying mechanism of the cross-modal responses. Here, we addressed this issue by applying fine-grained analyses of within- and cross-modal repetition suppression effects (RSEs) and Multi-Voxel Pattern Analyses in fMRI and sEEG experiments. Convergent evidence across analysis methods and protocols showed significant RSEs and successful decoding in both within-modal visual and auditory conditions suggesting that subpopulations of neurons within the left-vOT distinctly encode written and spoken language inputs. This functional organization of neural populations enables the area to respond to speech input directly and indirectly, i.e., after speech sounds are converted to orthographic representations. The finding opens further discussions on how the human brain may be prepared and adapted for an acquisition of a complex ability such as reading. Significance StatementLearning to read generates new functional responses in neurons in the left ventral visual pathway. Soon after reading acquisition, these neurons become specialized in processing known scripts, thus leading to the functional designation of the "Visual Word Form Area" (VWFA). However, controversies remain regarding the nature of neural representations encoded in this "reading" region, as its activation to speech is also reported. We investigate the neural mechanism(s) underlying these bimodal responses using within and cross-modal repetition suppression and decoding protocols. fMRI and sEEG experiments provided converging evidence indicating that, despite its specialization in reading, VWFA also contained subpopulations of neurons that encode speech. This functional organization could reveal why neurons at this anatomical location are ideal for reading acquisition.