Multimodal study of multilevel pulvino-temporal connections: a new piece in the puzzle of lexical retrieval networks

Brain. 2024 Jan 18:awae021. doi: 10.1093/brain/awae021. Online ahead of print.


Advanced methods of imaging and mapping the healthy and lesioned brain allowed to identify the cortical nodes and white matter tracts supporting the dual neurofunctional organization of language networks in a dorsal phonological and a ventral semantic stream. Much less understood are the anatomical correlates of the interaction between the two streams, one hypothesis being that of a sub-cortically mediated interaction, through crossed cortico-striato-thalamo-cortical and cortico-thalamo-cortical loops. In this regard, the pulvinar is the thalamic subdivision that has most regularly appeared as implicated in the processing of lexical retrieval. However, descriptions of its connections with temporal (language) areas remain scarce. Here we assess this pulvino-temporal connectivity using a combination of state-of-the-art techniques: white matter stimulation in awake surgery and post-operative diffusion MRI (n = 4), virtual dissection from the Human Connectome Project 3 T and 7 T datasets (n = 172), and operative microscope-assisted post-mortem fiber dissection (n = 12). We demonstrate the presence of four fundamental fiber contingents: i) the anterior component (Arnold's bundle proper) initially described by Arnold in the 19th century, and destined to the anterior temporal lobe; ii) the Optic Radiations (OR)-like component, that leaves the pulvinar accompanying the optical radiations and reaches the posterior basal temporal cortices; iii) the lateral component, that crosses orthogonally the temporal stem and reaches the middle temporal gyrus; and iv) the Auditory Radiations (AR)-like component, that leaves the pulvinar accompanying the auditory radiations to the superomedial aspect of the temporal operculum, just posteriorly to Heschl's gyrus. Each of those components might correspond to a different level of information processing involved in the lexical retrieval process of picture naming.

Keywords: diffusion imaging; lexical retrieval; low-grade glioma; pulvinar; temporal lobe; white matter.