Neuroanatomical Dissociation of Encoding Processes Related to Priming and Explicit Memory

Abstract

Priming is a facilitation of cognitive processing with stimulus repetition that can occur without explicit memory. Whereas the functional neuroanatomy of perceptual priming at retrieval is established, encoding processes that initiate priming and explicit memory have not yet been anatomically separated, and we investigated them using event-related functional magnetic resonance imaging. Activations predicting later explicit memory occurred in the bilateral medial temporal lobe (MTL) and left prefrontal cortex (PFC). Activity predicting later priming did not occur in these areas, but rather in the bilateral extrastriate cortex, left fusiform gyrus, and bilateral inferior PFC, areas linked with stimulus identification. Surprisingly, these regions showed response reductions. Our results demonstrate that priming and explicit memory have distinct functional neuroanatomies at encoding, with MTL activations being specific for explicit memory, and suggest that priming is initiated by sharpness of neural responding in stimulus identification areas, consistent with recent electrophysiological evidence regarding priming-related neural oscillations at encoding. We tentatively suggest that this sharpened responding at encoding may set the stage for increased neural processing efficiency at retrieval, with these different neural mechanisms both leading to observed priming-related hemodynamic decreases, and argue that neural measurements at encoding, and not just at retrieval, will be critical in resolving the debate about the neural mechanisms of learning that underlie priming.

Real-Time Neural Signals of Perceptual Priming with Unfamiliar Geometric Shapes

“…The priming Dm, right lateralized from ϳ200 -500 ms and bilateral from ϳ600 -900 ms, is consistent with a priming Dm found with fMRI, which included activity increases in parietal cortex especially on the right (Schott et al, 2006). Collectively, our results suggest that greater perceptual learning on the first encounter with a novel item (positive priming Dm) produces a memory representation that enables more fluent processing of the same item in a subsequent encounter (negative old/new effect).…”

“…The negative ERP effects attributed to priming were occipital in focus and onset rapidly, thus appearing as negative modulations of early, object-sensitive ERP components related to activity in object-sensitive visual cortex measured with fMRI (Schendan and Lucia, 2010). Furthermore, occipital-negative ERP effects similar to those reported here have been identified in conditions that also produce reductions in object-sensitive visual cortex activity measured with fMRI (Schott et al, 2002(Schott et al, , 2006. The available evidence thus fits well with the interpretation of priming-related negative ERP effects reported here as signals of reduced cortical activity, but direct evidence for this proposal should be provided by other means in future studies.…”

“…The present design thus allowed us to characterize electrophysiological correlates of perceptual priming while minimizing concurrent conceptual processing and explicit memory. We also assessed perceptual learning during initial kaleidoscope presentation by identifying ERPs that predicted later priming, as in prior studies that found differences between activity predictive of priming versus explicit memory for words (Paller et al, 1987b;Paller, 1990;Paller and Kutas, 1992;Schott et al, 2002Schott et al, , 2006.…”

Medial temporal theta state before an event predicts episodic encoding success in humans

“…Recent observations that perception of a stimulus can be influenced by prestimulus brain activity (10,11) raise the additional possibility that the brain state immediately preceding an event could predict later episodic memory. This possibility is supported by findings in rodents that the amplitude of hippocampal theta (3)(4)(5)(6)(7)(8) oscillations, which are held to be important modulators of the induction of synaptic plasticity (12)(13)(14), is associated with enhanced learning in classical conditioning even before stimulus onset (15)(16)(17). Because the medial temporal lobe (MTL) and, in particular, the hippocampus are also critical for episodic memory encoding in humans (18)(19)(20), prestimulus mediotemporal theta states might be linked to effective episodic memory encoding.…”

Spoken Word Memory Traces within the Human Auditory Cortex Revealed by Repetition Priming and Functional Magnetic Resonance Imaging

“…Repetition of familiar material usually entails a decrease in neuronal activity, referred to as repetition suppression, which may rely on a sharpened representation composed of neurons that code only key stimulus features (Desimone, 1996;Wiggs and Martin, 1998;Grill-Spector et al, 2006). Repetition suppression has been found in various visual areas (for review, see Schacter et al, 2004) coding written words (Schott et al, 2006), faces (Eger et al, 2005), objects (Vuilleumier et al, 2002) or line drawings (Lebreton et al, 2001). Repetition of unfamiliar material, however, sometimes leads to an increase in cortical activity (Schacter et al, 1995a;Habeck et al, 2006), referred to as repetition enhancement, which may reflect the formation of new cell assemblies (Henson, 2000;Fiebach et al, 2005).…”