Prefrontal-temporal circuitry for episodic encoding and subsequent memory

Abstract

Humans encounter and form memories for multiple types of experiences that differ in content, novelty, and memorability. Critical for understanding memory is determining (1) how the brain supports the encoding of events with differing content and (2) whether neural regions that are sensitive to novelty also influence whether stimuli will be subsequently remembered. This event-related functional magnetic resonance imaging (fMRI) study crossed content (picture/word), novelty (novel/repeated), and subsequent memory (remembered/forgotten) to examine prefrontal and temporal lobe contributions to encoding. Results revealed three patterns of encoding-related activation in anatomically connected inferior prefrontal and lateral temporal structures that appeared to vary depending on whether visuospatial/visuo-object, phonological/lexical, or semantic attributes were processed. Event content also modulated medial temporal lobe activity; word encoding predominantly activated the left hemisphere, whereas picture encoding activated both hemispheres. Critically, in prefrontal and temporal regions that were modulated by novelty, the magnitude of encoding activation also predicted whether an event would be subsequently remembered. These results suggest that (1) regions that demonstrate a sensitivity to novelty may actively support encoding processes that impact subsequent explicit memory and (2) multiple content-dependent prefrontal-temporal circuits support event encoding. The similarities between prefrontal and lateral temporal encoding responses raise the possibility that prefrontal modulation of posterior cortical representations is central to encoding.

Fig. 1.

Inferior prefrontal, fusiform, and left lateral temporal encoding responses. Columns A–E, Activity during novel stimulus (novel > repeated pictures + words), novel picture (novel > repeated), picture versus word (novel picture > novel word), novel word (novel > repeated), and word versus picture (novel word > novel picture) encoding, respectively. Regions of interest were defined from the novel stimulus (a–e), novel word (f), and word versus picture (g) comparisons. a, Anterior LIPC: −37, 25, 3; BA 45/47. b, Posterior LIPC: −34, 6, 34; BA 6/44. c, Posterior RIPC: 43, 3, 37; BA 6/44. d, Left posterior fusiform: −28, −55, −9; BA 37. e, Right posterior fusiform: 34, −49, −12; BA 37. f, Left lateral temporal cortex: −56, −43, 3; BA 21/22. g, Left anterior fusiform: −40, −43, −6; BA 37. L, Left; R, right.

Fig. 2.

Percent signal change time courses from the inferior prefrontal, fusiform, and left lateral temporal regions of interest shown in Figure 1 and labeled a–g. The posterior RIPC (c) and bilateral posterior fusiform regions (d, e) demonstrated picture preferential encoding responses, the posterior LIPC (b) and left anterior fusiform (g) demonstrated word preferential encoding responses, and the anterior LIPC (a) and left lateral temporal cortex (f) demonstrated word specific encoding responses.

Fig. 3.

Parahippocampal/fusiform regions engaged in novel stimulus encoding. Columns A–C represent novel stimulus, novel picture, and novel word comparisons, respectively. To compare the percent signal change responses to novel pictures and novel words in similar regions in both hemispheres, we used the coordinates from the left parahippocampal/ fusiform ROI in the novel stimulus condition to grow a region in the right hemisphere. a(−21, −40, −9; BA 35/36/37) and b (21, −40, −9; BA 35/36/37) reflect the percent signal change time courses from these ROIs. Picture and word encoding activated overlapping regions of the posterior MTL. Novel pictures, solid white line withwhite squares; repeated pictures, dashed white line with white squares; novel words,solid yellow line with yellow squares; repeated words, dashed yellow line with yellow squares.

Fig. 4.

Medial temporal regions that were more active during the encoding of pictures that were subsequently remembered than during the encoding of pictures that were subsequently forgotten.a, 28, −30, −6; hippocampus. b, −28, −37, −9; BA35/36/37. c, 31, −40, −6; BA 35/36/37. Graphs a–c, Subsequent memory percent signal change time courses. Graphs a₁–c₁, Novelty percent signal change time courses for the same ROIs depicted in a–c, respectively. Medial temporal regions that demonstrated picture subsequent memory effects also revealed picture and word novelty responses and trends for word subsequent memory effects. Graphs a–c, Remembered pictures, solid white line withwhite squares; forgotten pictures, dashed white line with white squares; remembered words,solid yellow line with yellow squares; forgotten words, dashed yellow line with yellow squares. Graphs a₁–c₁, Novel pictures, solid white line with white squares; repeated pictures, dashed white linewith white squares; novel words, solid yellow line with yellow squares; repeated words,dashed yellow line with yellow squares.