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.

Deconstructing the effect of self-directed study on episodic memory

“…The results from Voss, Gonsalves, et al (2011) showed an advantage for self-directed encoding for both recognition and spatial recall. A consistent pattern of results was found in a separate follow-up experiment, showing that the benefit from self-directed encoding was still evident a week after the initial study session (Voss, Galvan, et al, 2011). …”

“…A recent set of studies (Voss, Galvan, et al, 2011; Voss, Gonsalves, et al 2011; Voss, Warren, et al, 2011) found a robust benefit for self-directed memory encoding in a spatial exploration task in which participants memorized the identity and location of icons presented in a series of 5×5 grids (see Figure 1). At any given time, a single item in the grid was visible through a “window" that moved throughout the display.…”

“…Recent studies have shown that self-directed study leads to better episodic memory than passive observation in a variety of tasks, including face recognition (Liu, Ward, & Markall, 2007), object recognition (Harman, Humphrey, & Goodale, 1999; Voss, Galvan, & Gonsalves, 2011; Voss, Gonsalves, Federmeier, Tranel, & Cohen, 2011; Voss, Warren, et al, 2011), and spatial learning (Meijer & Van der Lubbe, 2011; Plancher, et al, 2012). Memory improvements have also been found in tasks where learners choose which items to study in preparation for future cued recall tests (Kornell & Metcalfe, 2006).…”

Active retrieval facilitates across-episode binding by modulating the content of memory

“…For instance, exerting volitional controlduring object-location learning facilitates later memory of the individual objects and the related spatial locations relative to passively viewing the objects in a predetermined sequence (Voss, Galvan, & Gonsalves, 2011; Voss, Gonsalves, Federmeier, Tranel, & Cohen, 2011; Voss, Warren, et al, 2011). Taken together, these findings suggest that methods to promote active retrieval could be used to enhance encoding of novel information.…”

“…It is unclear from the current results what brain regions are involved in this binding-related facilitation by active retrieval, although our previous experiment specifically implicated anterior hippocampus (Bridge & Voss, 2014). By further refining knowledge of critical brain regions in future studies, it will be possible to determine whether facilitation by active retrieval would be appropriate for use by individuals suffering from memory impairments due to damage to regions likely involved, such as hippocampus and prefrontal cortex (which are prominently involved in the influence of active retrieval and learning on memory; (Bridge & Voss, 2014 ; Voss, Gonsalves, et al, 2011; Voss, Warren, et al, 2011)). In summary, active retrieval has a unique promotional effect on integrating new information into existing memories, over and above passively encountering familiar information.…”