Unexpected novelty and familiarity orienting responses in lateral parietal cortex during recognition judgment

The role of lateral parietal cortex during recognition memory is heavily debated. We examined parietal activation during an Explicit Memory Cueing recognition paradigm that biases participants towards expecting novel or familiar stimuli on a trial-by-trial basis using anticipatory cues (“Likely Old”, “Likely New”), compared to trials with neutral cues (“????”). Three qualitatively distinct patterns were observed in the left lateral parietal cortex. An unexpected novelty response occurred in left anterior intraparietal cortex (IPS)/post-central gyrus (PoCG) in which greater activation was observed for new vs. old materials following the “Likely Old” cue, but not following the “Likely New” cue. In contrast, anterior angular gyrus demonstrated an unexpected familiarity response with greater activation for old vs. new materials following the “Likely New” cue, but not the “Likely Old” cue. Thus these two regions demonstrated increased responses that were selective for either new or old materials respectively, but only when they were unexpected. In contrast, a mid IPS area demonstrated greater response for whichever class of memoranda was unanticipated given the cue condition (an unexpected memory response). Analogous response patterns in regions outside of parietal cortex, and the results of a resting state connectivity analysis, suggested these three response patterns were associated with visuo-spatial orienting following unexpected novelty, source monitoring operations following unexpected familiarity, and general executive control processes following violated expectations. These findings support a Memory Orienting Model of the left lateral parietal cortex in which the region is linked to the investigation of unexpected novelty or familiarity in the environment.

► Violation of memory expectations activate posterior parietal cortex.
► Left posterior parietal cortex demonstrates functional heterogeneity in orienting responses.
► Left anterior IPS/post-central gyrus selectively responds to unexpected novelty.
► Left anterior angular gyrus selectively responds to unexpected familiarity.