Unconscious Learning versus Visual Perception: Dissociable Roles for Gamma Oscillations Revealed in MEG Maximilien Chaumon 1 , Denis Schwartz 2 , and Catherine Tallon-Baudry 1,2 Abstract & Oscillatory synchrony in the gamma band (30–120 Hz) has been involved in various cognitive functions including con- scious perception and learning. Explicit memory encoding, in particular, relies on enhanced gamma oscillations. Does this finding extend to unconscious memory encoding? Can we dissociate gamma oscillations related to unconscious learning and to conscious perception? We investigate these issues in a magnetoencephalographic experiment using a modified ver- sion of the contextual cueing paradigm. In this visual search task, repeated presentation of search arrays triggers an un- conscious spatial learning process that speeds reaction times but leaves conscious perception unaffected. In addition to a high-frequency perceptual gamma activity present throughout the experiment, we reveal the existence of a fronto-occipital network synchronized in the low gamma range specifically engaged in unconscious learning. This network shows up as soon as a display is searched for the second time and disap- pears as behavior gets affected. We suggest that oscillations in this network shape neural processing to build an efficient neural route for learned displays. Accordingly, in the last part of the experiment, evoked responses dissociate learned images at early latencies, suggesting that a sharpened representation is activated without resort on learning gamma oscillations, where- as perceptual gamma oscillations remain unaffected. & INTRODUCTION Learning is considered to rely on the modification of syn- apses and pathways: Training progressively builds a more efficient neural route through the modification of neural connectivity (Hebb, 1949). The mechanisms of synaptic plasticity underlying learning are highly sensitive to the precise timing of neural activity (Abbott & Nelson, 2000; Bi & Poo, 1998; Markram, Lubke, Frotscher, & Sakmann, 1997) and are more likely to take place upon repeated stimulation. Because oscillatory synchrony offers an oppor- tunity to control precisely the timing of pre- and postsyn- aptic activities and to repeat this precise temporal pattern at each oscillation cycle, it has long been suspected to be involved in learning and memory (Singer, 1995, 1999) and was recently observed during memory performance in ani- mals in the hippocampal region (Bauer, Paz, & Pare, 2007; Montgomery & Buzsaki, 2007; Csicsvari, Jamieson, Wise, & Buzsaki, 2003; Bragin et al., 1995) and in the neocortex (Stiefel, Tennigkeit, & Singer, 2005; Rodriguez, Kallenbach, Singer, & Munk, 2004; Wespatat, Tennigkeit, & Singer, 2004). Studies in humans suggest a role of induced gamma band (30–120 Hz, non-phase-locked to the stimulus) os- cillations in coupling perception and learning ( Jensen, Kaiser, & Lachaux, 2007). Memory encoding, under its simplest form, appears as a decrease (or sometimes in- crease) of neural activity upon repeated presentations of the same stimulus. This phenomenon, known as repeti- tion suppression (Grill-Spector, Henson, & Martin, 2006), can be specifically observed in the gamma band (Gruber & Mu ¨ller, 2002, 2005, 2006). Episodic memory encoding also seems to benefit from oscillatory synchrony: Enhanced gamma oscillations have been observed during the pre- sentation of an item when it is subsequently remem- bered compared to when it is forgotten (Osipova et al., 2006; Gruber, Tsivilis, Montaldi, & Mu ¨ller, 2004; Sederberg, Kahana, Howard, Donner, & Madsen, 2003; Fell et al., 2001). Last, higher levels of synchrony in the gamma band have also been observed in an operant condition- ing task (Miltner, Braun, Arnold, Witte, & Taub, 1999) and in a paired associate learning task (Gruber, Keil, & Mu ¨ller, 2001). These findings raise two questions. First, is induced gamma activity only involved in the formation of explicit memories or can it also be observed during unconscious learning? Second, how can one relate the role of in- duced gamma oscillations in learning with its role in visual perception (Tallon-Baudry & Bertrand, 1999)? In 1 Universite´ Pierre et Marie Curie (Paris6), LENA CNRS UPR640, Paris, France, 2 MEG-EEG Center, Ho ˆpitalde laPitie´-Salpe ˆtrie`re, Paris, France D 2008 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 21:12, pp. 2287–2299