Learning and Recognition of a Non-conscious Sequence of Events in Human Primary Visual Cortex

Human primary visual cortex (V1) has long been associated with learning simple low-level visual discriminations [1Sasaki Y. Nanez J.E. Watanabe T. Advances in visual perceptual learning and plasticity.Nat. Rev. Neurosci. 2010; 11: 53-60Crossref PubMed Scopus (270) Google Scholar] 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 [2Eichenbaum H. Yonelinas A.P. Ranganath C. The medial temporal lobe and recognition memory.Annu. Rev. Neurosci. 2007; 30: 123-152Crossref PubMed Scopus (1846) Google Scholar, 3Clark R.E. Recognition memory: an old idea given new life.Curr. Biol. 2013; 23: R725-R727Abstract Full Text Full Text PDF PubMed Scopus (12) Google Scholar]. 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., [4Albouy G. Sterpenich V. Balteau E. Vandewalle G. Desseilles M. Dang-Vu T. Darsaud A. Ruby P. Luppi P.-H. Degueldre C. et al.Both the hippocampus and striatum are involved in consolidation of motor sequence memory.Neuron. 2008; 58: 261-272Abstract Full Text Full Text PDF PubMed Scopus (311) Google Scholar]). 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. [5Squire L.R. Wixted J.T. Clark R.E. Recognition memory and the medial temporal lobe: a new perspective.Nat. Rev. Neurosci. 2007; 8: 872-883Crossref PubMed Scopus (760) Google Scholar]) and (2) align with mouse models of experience-dependent V1 plasticity in learning and memory [6Cooke S.F. Komorowski R.W. Kaplan E.S. Gavornik J.P. Bear M.F. Visual recognition memory, manifested as long-term habituation, requires synaptic plasticity in V1.Nat. Neurosci. 2015; 18: 262-271Crossref PubMed Scopus (73) Google Scholar].