Semantic Congruence Accelerates the Onset of the Neural Signals of Successful Memory Encoding

Abstract

As the stream of experience unfolds, our memory system rapidly transforms current inputs into long-lasting meaningful memories. A putative neural mechanism that strongly influences how input elements are transformed into meaningful memory codes relies on the ability to integrate them with existing structures of knowledge or schemas. However, it is not yet clear whether schema-related integration neural mechanisms occur during online encoding. In the current investigation, we examined the encoding-dependent nature of this phenomenon in humans. We showed that actively integrating words with congruent semantic information provided by a category cue enhances memory for words and increases false recall. The memory effect of such active integration with congruent information was robust, even with an interference task occurring right after each encoding word list. In addition, via electroencephalography, we show in 2 separate studies that the onset of the neural signals of successful encoding appeared early (ϳ400 ms) during the encoding of congruent words. That the neural signals of successful encoding of congruent and incongruent information followed similarly ϳ200 ms later suggests that this earlier neural response contributed to memory formation. We propose that the encoding of events that are congruent with readily available contextual semantics can trigger an accelerated onset of the neural mechanisms, supporting the integration of semantic information with the event input. This faster onset would result in a long-lasting and meaningful memory trace for the event but, at the same time, make it difficult to distinguish it from plausible but never encoded events (i.e., related false memories).

The congruence effect is impaired in healthy aging: a relationship to event-related potentials and theta-alpha oscillations

“…Experimental stimuli consisted of 66 categorical 6 word lists (Packard et al, 2016) translated into German, selected from category norms (Battig and Montague, 1969;Kim and Cabeza, 2007a;Yoon et al, 2004).…”

“…Finally, bad channels were interpolated. Oz was selected to re-reference the data, as re-referencing to average can mask the effects of EEG differences with a broad distribution across the scalp (Luck, 2005), such as we expected following previous experiments (Packard et al, 2016). EEG trials with a shift exceeding 100 V were rejected offline.…”

“…Long-term memory can be improved by presenting the information that has to be learned within a known context. In humans, this has often been demonstrated with a priori semantic information followed by congruent (vs. incongruent) material, and has, therefore, been labeled semantic congruence effect (or simply 'congruence effect') (Atienza et al, 2011;Craik and Tulving, 1975;Hall and Geis, 1980;Kapur et al, 1994;Packard et al, 2016;Schulman, 1974;Tse et al, 2011Tse et al, , 2007. While most previous studies have focused on younger participants (i.e.…”

“…Post-stimulus event-related potentials (ERP) during encoding reflect memory processes that are modulated by earlier input or the configuration of activity in memory (Federmeier and Laszlo, 2009;Friedman and Johnson, 2000). Specifically, semantic congruence not only drives long-term memory, as described above, but it also modulates early encoding-related post-stimulus positive ERPs (Packard et al, 2016). During healthy aging, decreases in ERPs associated with semantic congruence reflect an age-related deterioration in neural mechanisms (Huang et al, 2012;Kutas and Iragui, 1998;Wlotko et al, 2010) causing declines in encoding (Daselaar et al, 2003;Friedman et al, 1996;Glisky et al, 2001;Kamp and Zimmer, 2015;Logan et al, 2002).…”

“…Here, we used electroencephalography (EEG) to investigate the neural mechanisms involved in the agerelated differences in the semantic congruence effect. To this end, we implemented an adapted word list paradigm from a previous study (Packard et al, 2016), in which a strong memory enhancement was found for congruent words, with a corresponding early appearing ERP during encoding. Participants were presented with a series of word pairs: the first word was a semantic category (e.g.…”