Expectation-Driven Changes in Cortical Functional Connectivity Influence Working Memory and Long-Term Memory Performance

Abstract

Expectations generated by predictive cues increase the efficiency of perceptual processing for complex stimuli (e.g., faces, scenes); however, the impact this has on working memory (WM) and long-term memory (LTM) has not yet been investigated. Here, healthy young adults performed delayed-recognition tasks that differed only in stimulus category expectations, while behavioral and functional magnetic resonance imaging data were collected. Univariate and functional-connectivity analyses were used to examine expectation-driven, prestimulus neural modulation, networks that regulate this modulation, and subsequent memory performance. Results revealed that predictive category cueing was associated with both enhanced WM and LTM for faces, as well as baseline activity shifts in a face-selective region of the visual association cortex [i.e., fusiform face area (FFA)]. In addition, the degree of functional connectivity between FFA and right inferior frontal junction (IFJ), middle frontal gyrus (MFG), inferior frontal gyrus, and intraparietal sulcus correlated with the magnitude of prestimulus activity modulation in the FFA. In an opposing manner, prestimulus connectivity between FFA and posterior cingulate cortex, a region of the default network, negatively correlated with FFA activity modulation. Moreover, whereas FFA connectivity with IFJ and the precuneus predicted enhanced expectation-related WM performance, FFA connectivity with MFG predicted LTM improvements. These findings suggest a model of expectancy-mediated neural biasing, in which a single node (e.g., FFA) can be dynamically linked or disconnected from different brain regions depending on prestimulus expectations, and the strength of distinct connections is associated with WM or LTM benefits.

When Anticipation Aids Long-Term Memory: What Cognitive and Neural Processes Are Involved?

“…Interestingly, Bollinger et al (2010) showed that predictive cues enhanced memory for faces but not for scenes. This result mirrored fMRI data reported by the authors.…”

“…As a consequence, the relationship between anticipation and LTM could be assessed at the neural level (for example, contrasting anticipatory brain activity for items that were later remembered with items that were later forgotten), but the effects of anticipation on LTM performance could not be directly assessed. Comparing cues with different degrees of predictability enables one to investigate the effectiveness of anticipation on behavior; this approach should be useful for future research.Interestingly, Bollinger et al (2010) showed that predictive cues enhanced memory for faces but not for scenes. This result mirrored fMRI data reported by the authors.…”

“…In a recent report published in The Journal of Neuroscience, Bollinger et al (2010) demonstrated that both working memory (WM) and long-term memory (LTM) benefit from anticipation of a stimulus from a given category. Participants were instructed to memorize faces or scenes in a delayed matching-to-sample task.…”

“…This analysis approach uses trial-by-trial variability to measure correlations in activity between different brain regions. Bollinger et al (2010) showed that FFA activity following face-predicting cues was functionally connected with a network of frontoparietal regions that are thought to bias sensory processing of expected stimuli. Connectivity measures between these regions and the FFA were then correlated with WM and LTM performance.…”

“…The authors reported that WM performance was positively correlated with increased functional connectivity between the FFA, the right inferior frontal gyrus, and the left precuneus, whereas LTM performance was correlated with increased functional connectivity between the FFA and the left middle frontal gyrus. Bollinger et al (2010) suggested that top-down signals bias processing in visual-selective regions when foreknowledge about the stimulus is available. The authors have convincingly shown that this mechanism may benefit WM and LTM performance.…”