An ERP measure of non-conscious memory reveals dissociable implicit processes in human recognition using an open-source automated analytic pipeline.

Non-conscious processing of human memory has traditionally been difficult to objectively measure and thus understand. A prior study on a group of hippocampal amnesia (N = 3) patients and healthy controls (N = 6) used a novel procedure for capturing neural correlates of implicit memory using event-related potentials (ERPs): old and new items were equated for varying levels of memory awareness, with ERP differences observed from 400 to 800 ms in bilateral parietal regions that were hippocampal-dependent. The current investigation sought to address the limitations of that study by increasing the sample of healthy subjects (N = 54), applying new controls for construct validity, and developing an improved, open-source tool for automated analysis of the procedure used for equating levels of memory awareness. Results faithfully reproduced prior ERP findings of parietal effects that a series of systematic control analyses validated were not contributed to nor contaminated by explicit memory. Implicit memory effects extended from 600 to 1000 ms, localized to right parietal sites. These ERP effects were found to be behaviorally relevant and specific in predicting implicit memory response times, and were topographically dissociable from other traditional ERP measures of implicit memory (miss vs. correct rejections) that instead occurred in left parietal regions. Results suggest first that equating for reported awareness of memory strength is a valid, powerful new method for revealing neural correlates of non-conscious human memory, and second, behavioral correlations suggest that these implicit effects reflect a pure form of priming, whereas misses represent fluency leading to the subjective experience of familiarity.

Neural correlates of the Dunning-Kruger effect.

The Dunning-Kruger effect (DKE) is a metacognitive phenomenon of illusory superiority in which individuals who perform poorly on a task believe they performed better than others, yet individuals who performed very well believe they under-performed compared to others. This phenomenon has yet to be directly explored in episodic memory, nor explored for physiological correlates or reaction times. We designed a novel method to elicit the DKE via a test of item recognition while electroencephalography (EEG) was recorded. Throughout the task, participants were asked to estimate the percentile in which they performed compared to others. Results revealed participants in the bottom 25th percentile over-estimated their percentile, while participants in the top 75th percentile under-estimated their percentile, exhibiting the classic DKE. Reaction time measures revealed a condition-by-group interaction whereby over-estimators responded faster than under-estimators when estimating being in the top percentile and responded slower when estimating being in the bottom percentile. Between-group EEG differences were evident between over-estimators and under-estimators during Dunning-Kruger responses, which revealed FN400-like effects of familiarity supporting differences for over-estimators, whereas "old-new" memory event-related potential effects revealed a late parietal component associated with recollection-based processing for under-estimators that was not evident for over-estimators. Findings suggest over- and under-estimators use differing cognitive processes when assessing their performance, such that under-estimators may rely on recollection during memory while over-estimators may draw upon excess familiarity when over-estimating their performance. Episodic memory thus appears to play a contributory role in metacognitive judgements of illusory superiority.

Recallable but not recognizable: The influence of semantic priming in recall paradigms.

When people can successfully recall a studied word, they should be able to recognize it as having been studied. In cued-recall paradigms, however, participants sometimes correctly recall words in the presence of strong semantic cues but then fail to recognize those words as actually having been studied. Although the conditions necessary to produce this unusual effect are known, the underlying neural correlates have not been investigated. Across five experiments, involving both behavioral and electrophysiological methods (EEG), we investigated the cognitive and neural processes that underlie recognition failures. Experiments 1 and 2 showed behaviorally that assuming that recalled items can be recognized in cued-recall paradigms is a flawed assumption, because recognition failures occur in the presence of cues, regardless of whether those failures are measured. With event-related potentials (ERPs), Experiments 3 and 4 revealed that successfully recalled words that are recognized are driven by recollection at recall and then by a combination of recollection and familiarity at ensuing recognition. In contrast, recognition failures did not show that memory signature and may instead be driven by semantic priming at recall and followed at recognition stages by negative-going ERP effects consistent with implicit processes, such as repetition fluency. These results demonstrate that recall - long-characterized as predominantly reflecting recollection-based processing in episodic memory - may at times also be served by a confluence of implicit cognitive processes.

Neurophysiological evidence that perceptions of fluency produce mere exposure effects.

Recent exposure to people or objects increases liking ratings, the "mere exposure effect" (Zajonc in American Psychologist, 35, 117-123, 1968), and an increase in processing fluency has been identified as a potential mechanism for producing this effect. This fluency hypothesis was directly tested by altering the trial-by-trial image clarity (i.e., fluency) while Event-Related Potentials (ERPs) were recorded. In Experiment 1, clarity was altered across two trial blocks that each had homogenous trial-by-trial clarity, whereas clarity varied randomly across trials in Experiment 2. Blocking or randomizing image clarity across trials was expected to produce different levels of relative fluency and alter mere exposure effects. The mere exposure effect (i.e., old products liked more than new products) was observed when stimulus clarity remained constant across trials, and clear image ERPs were more positive than blurry image ERPs. Importantly, these patterns were reversed when clarity varied randomly across test trials, such that participants liked clear images more than blurry (i.e., no mere exposure effect) and clear image ERPs were more negative than blurry image ERPs. The findings provide direct experimental support from both behavioral and electrophysiological measures that, in some contexts, mere exposure is the product of top-down interpretations of fluency.

Prestimulus theta activity predicts correct source memory retrieval.

Recent evidence indicates that the processing of a stimulus can be influenced by preceding patterns of brain activity. Here we examine whether prestimulus oscillatory brain activity can influence the ability to retrieve episodic memories. Neural activity in the theta-frequency band (4-8 Hz) was enhanced before presentation of test items which elicited accurate recollection of contextual details of the prior study episode ("source retrieval"), relative to trials for which item recognition was successful but source retrieval failed. Poststimulus theta activity was also related to source retrieval, and the magnitude of poststimulus theta was predicted by the magnitude of the prestimulus theta effects. The results suggest that ongoing neural processes occurring before stimulus onset might play a critical role in readying the brain for successful memory retrieval.

Examining ERP correlates of recognition memory: evidence of accurate source recognition without recollection.

Recollection is typically associated with high recognition confidence and accurate source memory. However, subjects sometimes make accurate source memory judgments even for items that are not confidently recognized, and it is not known whether these responses are based on recollection or some other memory process. In the current study, we measured event related potentials (ERPs) while subjects made item and source memory confidence judgments in order to determine whether recollection supported accurate source recognition responses for items that were not confidently recognized. In line with previous studies, we found that recognition memory was associated with two ERP effects: an early on-setting FN400 effect, and a later parietal old-new effect [late positive component (LPC)], which have been associated with familiarity and recollection, respectively. The FN400 increased gradually with item recognition confidence, whereas the LPC was only observed for highly confident recognition responses. The LPC was also related to source accuracy, but only for items that had received a high confidence item recognition response; accurate source judgments to items that were less confidently recognized did not exhibit the typical ERP correlate of recollection or familiarity, but rather showed a late, broadly distributed negative ERP difference. The results indicate that accurate source judgments of episodic context can occur even when recollection fails.

BOOSTING BRAIN WAVES IMPROVES MEMORY.

Have you ever wanted to improve your memory? Or have you struggled to remember what you studied? Memory uses special patterns of activity in the brain. This experiment tested a new way to create brain wave patterns that help with memory. We wanted to see if we could improve memory by using lights and sounds that teach the brain waves to be in sync. People wore special goggles that made flashes of light and headphones that made beeping noises. This trained the brain through a process called entrainment. The entrainment put the brain in sync at a specific brain wave pattern called theta. People whose brains were trained to be in theta had better memory compared to people whose brains did not get trained. We learned that entrainment is a cool new way to make memory better.

Entrainment enhances theta oscillations and improves episodic memory.

Neural oscillations in the theta band have been linked to episodic memory, but it is unclear whether activity patterns that give rise to theta play a causal role in episodic retrieval. Here, we used rhythmic auditory and visual stimulation to entrain neural oscillations to assess whether theta activity contributes to successful memory retrieval. In two separate experiments, human subjects studied words and were subsequently tested on memory for the words ('item recognition') and the context in which each had been previously studied ('source memory'). Between study and test, subjects in the entrainment groups were exposed to audiovisual stimuli designed to enhance activity at 5.5 Hz, whereas subjects in the control groups were exposed to white noise (Expt. 1) or 14 Hz entrainment (Expt. 2). Theta entrainment selectively increased source memory performance in both studies. Electroencephalography (EEG) data in Expt. 2 revealed that theta entrainment resulted in band-specific enhancement of theta power during the entrainment period and during post-entrainment memory retrieval. These results demonstrate a direct link between theta activity and episodic memory retrieval. Targeted manipulation of theta activity could be a promising new approach to enhance theta activity and memory performance in healthy individuals and in patients with memory disorders.

Event-related potential evidence for multiple causes of the revelation effect.

Asking people to discover the identity of a recognition test probe immediately before making a recognition judgment increases the probability of an old judgment. To inform theories of this "revelation effect," event-related potentials (ERPs) were recorded for revealed and intact test items across two experiments. In Experiment 1, we used a revelation effect paradigm where half of the test probes were presented as anagrams (i.e., a related task) and the other items were presented intact. The pattern of ERP results from this experiment suggested that revealing an item decreases initial familiarity levels and caused the revealed items to elicit similar levels of activity. In Experiment 2, half of the probes were preceded by an addition task (i.e., an unrelated task). The pattern of ERP effects in this study were distinct from those observed in Experiment 1. More specifically, revealed item ERPs were more negative than intact ERPs at frontal electrodes and more positive at parietal electrodes early in the interval. Later in the epoch, revealed item ERPs were more negative than intact items. These data suggest that related tasks decrease familiarity and alter the signal-to-noise ratio of old and new items, whereas unrelated tasks affect processing in a different way (perhaps by changing decision processes) that also results in the revelation effect. The implications for current theories of the revelation effect are discussed.