title: Learning and Recognition of a Non-conscious Sequence of Events in Human Primary Visual Cortex.
abstract: Human primary visual cortex (V1) has long been associated with learning simple low-level visual discriminations [1] and is classically considered outside of neural systems that support high-level cognitive behavior in contexts that differ from the original conditions of learning, such as recognition memory [2, 3]. Here, we used a novel fMRI-based dichoptic masking protocol-designed to induce activity in V1, without modulation from visual awareness-to test whether human V1 is implicated in human observers rapidly learning and then later (15-20 min) recognizing a non-conscious and complex (second-order) visuospatial sequence. Learning was associated with a change in V1 activity, as part of a temporo-occipital and basal ganglia network, which is at variance with the cortico-cerebellar network identified in prior studies of "implicit" sequence learning that involved motor responses and visible stimuli (e.g., [4]). Recognition memory was associated with V1 activity, as part of a temporo-occipital network involving the hippocampus, under conditions that were not imputable to mechanisms associated with conscious retrieval. Notably, the V1 responses during learning and recognition separately predicted non-conscious recognition memory, and functional coupling between V1 and the hippocampus was enhanced for old retrieval cues. The results provide a basis for novel hypotheses about the signals that can drive recognition memory, because these data (1) identify human V1 with a memory network that can code complex associative serial visuospatial information and support later non-conscious recognition memory-guided behavior (cf. [5]) and (2) align with mouse models of experience-dependent V1 plasticity in learning and memory [6].
authors.affiliation: Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX3 9DU, England, UK. Electronic address: clive.rosenthal@clneuro.ox.ac.uk.
authors.forename: Clive R
authors.initials: CR
authors.lastname: Rosenthal
authors.affiliation: Department of Experimental Psychology, University of Oxford, Oxford OX1 3UD, England, UK.
authors.forename: Samantha K
authors.initials: SK
authors.lastname: Andrews
authors.affiliation: Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX3 9DU, England, UK.
authors.forename: Chrystalina A
authors.initials: CA
authors.lastname: Antoniades
authors.affiliation: Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX3 9DU, England, UK.
authors.forename: Christopher
authors.initials: C
authors.lastname: Kennard
authors.affiliation: Basque Center on Cognition, Brain and Language, Paseo Mikeletegi, 20009 San Sebastian - Donostia, Spain; Ikerbasque, Basque Foundation for Science, 48013 Bilbao, Spain. Electronic address: d.soto@bcbl.eu.
authors.forename: David
authors.initials: D
authors.lastname: Soto
mesh_terms: D006624:Hippocampus / Q000502:physiology; D006801:Humans; D008279:Magnetic Resonance Imaging; D008568:Memory / Q000502:physiology*; D033281:Nontherapeutic Human Experimentation; D010775:Photic Stimulation; D014793:Visual Cortex / Q000502:physiology*; D014796:Visual Perception / Q000502:physiology
keywords: hippocampus; implicit; non-conscious memory; primary visual cortex; recognition memory; relational; sequence learning