Imaging 'top-down' mobilization of visual information: a case study in a posterior split-brain patient

During visual perception, automatic bottom-up and controlled top-down processes occur simultaneously and interact in a complex way, making them difficult to isolate and characterize. In rare neurological conditions, such a dissociation can be achieved more easily. In the present work, we studied a patient (AC) with a posterior lesion of the corpus callosum (CC), using a combination of behavioural, structural MRI and high-density scalp EEG measures. Given the complete disruption of the posterior half of the CC, we speculated that inter-hemispheric transfer of visual information was only possible through top-down mobilization across the preserved anterior segment of the CC. We designed a matching-to-sample visual task during which this patient was randomly presented with two successive numerical targets (T1 and T2) flashed with either a short or a long stimulus-onset asynchrony (SOA), each presented within one visual hemifield (HF). Intra-hemispheric processing of visual stimuli was essentially preserved. In sharp contrast, patient's performance was massively impaired during inter-HFs trials with a short-SOA, confirming the lack of fast inter-hemispheric transfer. Crucially, patient AC spontaneously improved his performance in inter-HFs trials with a long-SOA. This behavioral improvement was correlated with a mid-frontal ERP effect occurring during the T1-T2 interval, concomitant with an increase of functional connectivity of this region with distant areas including occipital regions. These results put to light a slow, non-automatic, and frontally mediated route of inter-hemispheric transfer dependent on top-down control.