Neural substrates of saccadic adaptation: Plastic changes versus error processing and forward versus backward learning

• Published in: NeuroImage (Orlando, Fla.) Fla.), 2022-11, Vol.262, p.119556-119556, Article 119556
• Main Authors: Métais, Camille, Nicolas, Judith, Diarra, Moussa, Cheviet, Alexis, Koun, Eric, Pélisson, Denis
• Format: Article
• Language: English
• Subjects: Adaptation; Brain mapping; Cerebellum; Cerebral cortex; Clinical trials; Cognition; Cognitive science; Cortex (cingulate); Cortex (parietal); Experiments; Eye movements; fMRI; Functional magnetic resonance imaging; Globus pallidus; Hemispheric laterality; Hypotheses; Localization; Neural plasticity; Neuroimaging; Occipital lobe; Oculomotor error; Saccadic eye movements; Sensorimotor adaptation; Signal processing; Target jumps
• ISSN: 1053-8119; 1095-9572
• DOI: 10.1016/j.neuroimage.2022.119556

•Cortical substrates of saccadic plasticity and error processing are still unknown.•Our fMRI study shows substrates specific to plasticity processes & error processing.•Distinct neural substrates are also found for the two directions of adaptation.•Findings emphasize the link between saccadic plasticity and spatial cognition. Previous behavioral, clinical, and neuroimaging studies suggest that the neural substrates of adaptation of saccadic eye movements involve, beyond the central role of the cerebellum, several, still incompletely determined, cortical areas. Furthermore, no neuroimaging study has yet tackled the differences between saccade lengthening (“forward adaptation”) and shortening (“backward adaptation”) and neither between their two main components, i.e. error processing and oculomotor changes. The present fMRI study was designed to fill these gaps. Blood-oxygen-level-dependent (BOLD) signal and eye movements of 24 healthy volunteers were acquired while performing reactive saccades under 4 conditions repeated in short blocks of 16 trials: systematic target jump during the saccade and in the saccade direction (forward: FW) or in the opposite direction (backward: BW), randomly directed FW or BW target jump during the saccade (random: RND) and no intra-saccadic target jump (stationary: STA). BOLD signals were analyzed both through general linear model (GLM) approaches applied at the whole-brain level and through sensitive Multi-Variate Pattern Analyses (MVPA) applied to 34 regions of interest (ROIs) identified from independent 'Saccade Localizer’ functional data. Oculomotor data were consistent with successful induction of forward and backward adaptation in FW and BW blocks, respectively. The different analyses of voxel activation patterns (MVPAs) disclosed the involvement of 1) a set of ROIs specifically related to adaptation in the right occipital cortex, right and left MT/MST, right FEF and right pallidum; 2) several ROIs specifically involved in error signal processing in the left occipital cortex, left PEF, left precuneus, Medial Cingulate cortex (MCC), left inferior and right superior cerebellum; 3) ROIs specific to the direction of adaptation in the occipital cortex and MT/MST (left and right hemispheres for FW and BW, respectively) and in the pallidum of the right hemisphere (FW). The involvement of the left PEF and of the (left and right) occipital cortex were further supported and qualified by the whole brain GLM analysis: clusters of inc