Cortical regions recruited for complex active-learning strategies and action planning exhibit rapid reactivation during memory retrieval

Abstract

Memory retrieval can involve activity in the same sensory cortical regions involved in perception of the original event, and this neural "reactivation" has been suggested as an important mechanism of memory retrieval. However, it is still unclear if fragments of experience other than sensory information are retained and later reactivated during retrieval. For example, learning in non-laboratory settings generally involves active exploration of memoranda, thus requiring the generation of action plans for behavior and the use of strategies deployed to improve subsequent memory performance. Is information pertaining to action planning and strategic processing retained and reactivated during retrieval? To address this question, we compared ERP correlates of memory retrieval for objects that had been studied in an active manner involving action planning and strategic processing to those for objects that had been studied passively. Memory performance was superior for actively studied objects, and unique ERP retrieval correlates for these objects were identified when subjects remembered the specific spatial locations at which objects were studied. Early-onset frontal shifts in ERP correlates of retrieval were noted for these objects, which parallel the recruitment of frontal cortex during learning object locations previously identified using fMRI with the same paradigm. Notably, ERPs during recall for items studied with a specific viewing strategy localized to the same supplementary motor cortex region previously identified with fMRI when this strategy was implemented during study, suggesting rapid reactivation of regions directly involved in strategic action planning. Collectively, these results implicate neural populations involved in learning in important retrieval functions, even for those populations involved in strategic control and action planning. Notably, these episodic features are not generally reported during recollective experiences, suggesting that reactivation is a more general property of memory retrieval that extends beyond those fragments of perceptual information that might be needed to re-live the past.

Figure 1. Effects of active learning on memory performance

(A) Subjects studied objects arranged on a grid via a restricted-viewing paradigm that permitted study of one object at a time through a viewing window. (B) Study was controlled via a computer mouse used to move the viewing window in the active condition, and no control was provided in the passive condition (i.e., the viewing window moved and subjects merely watched). The visual information available in both conditions was matched via a subject-to-subject yoking procedure. (C) Endorsement rates are provided for the subsequent recognition memory test, separately for each stimulus type (active-studied, passive-studied, new) and response type (remember location, remember other, know, and new). Error bars indicate SE.

Figure 2. Electrophysiological correlates of memory retrieval

(A) ERPs for active-studied and passive-studied objects endorsed with remember-location responses and for correctly rejected new objects are shown for two representative electrode locations marked on the cartoon plot of the head. The scalebar indicates 5μV, and positive is plotted up. Topographic plots of the old—new ERP difference are shown in 200 ms intervals starting at stimulus onset. Coloration indicates ERP difference amplitude (μV). The head is shown from a superior view, with anterior facing upward. (B) The same information is provided for active-studied and passive-studied objects endorsed with remember-other responses. (C) The same information is provided for active-studied and passive-studied objects endorsed with know responses. Gray background coloration on topographic plots indicates latency intervals for which any significant old/new differences were identified. Black lines with ≠ symbols indicate significantly different ERP topographies for the active and passive conditions.

Figure 3. Estimated neural sources of ERP reactivation effects

Estimated sources are shown for the influences of active versus passive learning on ERP correlates of remember-location responses. Results from each latency interval are shown in A—E, superimposed on a template brain shown laterally for left and right hemispheres and superiorly (with anterior oriented upward). Red coloration indicates the estimated maxima for each latency interval. Maxima for the 0–200 ms interval (A) included left and right Brodmann Area (BA) 8/9 spanning the middle and superior frontal gyri (Talairach coordinates −30, +40, +36 and +25, +38, +43, respectively). For the 200–400 ms interval (B), the maximum was left superior parietal lobule (BA 7, Talairach coordinates −24, −69, +57). For the 400–600 ms interval (C), maxima included left and right medial superior frontal gyrus (BA 6, Talairach coordinates −3, −8, +69 and +6, −11, +69, respectively) as well as more anterior left and right medial frontal gyrus (BA 8, Talairach coordinates −3, +38, +42 and +4, +39, +41, respectively). The maximum for the 600–800 ms interval (D) included right superior frontal gyrus (BA 6/8/9, Talairach coordinates +25, +39, +43). The maximum for the 800–1,000 ms interval (E) included approximately the same region of left superior frontal cortex as shown in A (BA 8/9, Talairach coordinates −27, +31, +43).

Figure 4. ERP reactivation related to the revisitation study strategy

(A) ERPs for actively studied objects given remember-location responses are shown separately for revisitation-studied and other-studied objects for two representative electrode locations marked on the cartoon plot of the head. The scalebar indicates 5μV, and positive is plotted up. (B) Topographic plots of the revisitation—other ERP difference are shown in 200 ms intervals starting at stimulus onset. Coloration indicates ERP difference amplitude (μV). The head is shown from a superior view, with anterior facing upward. Gray background coloration indicates latency intervals for which any significant old/new differences were identified. (C) Estimates sources for the revisitation—other ERP difference from 600–800 ms are shown superimposed on the medial aspect of a template brain. Red coloration indicates the estimated maxima for each latency interval. The supplementary motor cortex (more anterior) activation maximum was identified at Talairach coordinates −6, +30, +47 for the left hemisphere and +7, +31+43 for the right hemisphere. The primary motor cortex (more posterior) activation maximum was identified at Talairach coordinates −3, −11, +70 for the left hemisphere and +4, −10, +65 for the right hemisphere. (D) A red sphere (radius = 8 mm) is shown centered on the maximum of the left-hemisphere supplementary motor cortex estimated source and a yellow sphere (same radius) is shown centered on the supplementary motor cortex maximum defined as revisitation-related fMRI activity during study (Figure 4A of Voss, Warren, et al., 2011), both superimposed on a template brain.