Recognition memory and prefrontal cortex: dissociating recollection and familiarity processes using rTMS

Recognition memory can be supported by both the assessment of the familiarity of an item and by the recollection of the context in which an item was encountered. The neural substrates of these memory processes are controversial. To address these issues we applied repetitive transcranial magnetic stimulation (rTMS) over the right and left dorsolateral prefrontal cortex (DLPFC) of healthy subjects performing a remember/know task. rTMS disrupted familiarity judgments when applied before encoding of stimuli over both right and left DLPFC. rTMS disrupted recollection when applied before encoding of stimuli over the right DLPFC. These findings suggest that the DLPFC plays a critical role in recognition memory based on familiarity as well as recollection.     

Short theta burst stimulation to left frontal cortex prior to encoding enhances subsequent recognition memory

Deep semantic encoding of verbal stimuli can aid in later successful retrieval of those stimuli from long-term episodic memory. Evidence from numerous neuropsychological and neuroimaging experiments demonstrate regions in left prefrontal cortex, including left dorsolateral prefrontal cortex (DLPFC), are important for processes related to encoding. Here, we investigated the relationship between left DLPFC activity during encoding and successful subsequent memory with transcranial magnetic stimulation (TMS). In a pair of experiments using a 2-session within-subjects design, we stimulated either left DLPFC or a control region (Vertex) with a single 2-s train of short theta burst stimulation (sTBS) during a semantic encoding task and then gave participants a recognition memory test. We found that subsequent memory was enhanced on the day left DLPFC was stimulated, relative to the day Vertex was stimulated, and that DLPFC stimulation also increased participants’ confidence in their decisions during the recognition task. We also explored the time course of how long the effects of sTBS persisted. Our data suggest 2 s of sTBS to left DLPFC is capable of enhancing subsequent memory for items encoded up to 15 s following stimulation. Collectively, these data demonstrate sTBS is capable of enhancing long-term memory and provide evidence that TBS protocols are a potentially powerful tool for modulating cognitive function.     

The role of semantically related distractors during encoding and retrieval of words in long-term memory

We examined the influence of divided attention (DA) on recognition of words when the concurrent task was semantically related or unrelated to the to-be-recognised target words. Participants were asked to either study or retrieve a target list of semantically related words while simultaneously making semantic decisions (i.e., size judgements) to another set of related or unrelated words heard concurrently. We manipulated semantic relatedness of distractor to target words, and whether DA occurred during the encoding or retrieval phase of memory. Recognition accuracy was significantly diminished relative to full attention, following DA conditions at encoding, regardless of relatedness of distractors to study words. However, response times (RTs) were slower with related compared to unrelated distractors. Similarly, under DA at retrieval, recognition RTs were slower when distractors were semantically related than unrelated to target words. Unlike the effect from DA at encoding, recognition accuracy was worse under DA at retrieval when the distractors were related compared to unrelated to the target words. Results suggest that availability of general attentional resources is critical for successful encoding, whereas successful retrieval is particularly reliant on access to a semantic code, making it sensitive to related distractors under DA conditions.     

The effect of bicephalic stimulation of the dorsolateral prefrontal cortex on the attentional bias for threat: A transcranial direct current stimulation study

Previous stimulation studies demonstrated that the dorsolateral prefrontal cortex (DLPFC) is involved in threat processing. According to a model of emotional processing, an unbalance between the two DLPFCs, with a hyperactivation of right frontal areas, is involved in the processing of negative emotions and genesis of anxiety. In the present study, we investigated the role of the right and left DLPFC in threat processing in healthy women who also completed the State-Trait Anxiety Inventory (STAI). We simultaneously modulated the activity of the right and left dorsolateral prefrontal cortex by applying bicephalic transcranial direct current stimulation (tDCS) before participants completed a modified version of the classic Posner task using threatening and nonthreatening stimuli as spatial cues. Anodal stimulation on the right DLPFC with a simultaneous cathodal stimulation over the left side induced a disengagement bias in individuals with low STAI scores and a facilitation bias in individuals with high STAI scores. Anodal stimulation on the left DLPFC with the simultaneous cathodal stimulation over the right side did not affect threat processing. The findings of the present study provided specific support to the hypothesis that unbalanced activation between left and right hemispheres with enhanced activation of the right DLPFC is critical in early top-down threat processing in healthy individuals.     

Spatiotemporal competition and task-relevance shape the spatial distribution of emotional interference during rapid visual processing: Evidence from gaze-contingent eye-tracking

People’s ability to perceive rapidly presented targets can be disrupted both by voluntary encoding of a preceding target and by spontaneous attention to salient distractors. Distinctions between these sources of interference can be found when people search for a target in multiple rapid streams instead of a single stream: voluntary encoding of a preceding target often elicits subsequent perceptual lapses across the visual field, whereas spontaneous attention to emotionally salient distractors appears to elicit a spatially localized lapse, giving rise to a theoretical account suggesting that emotional distractors and subsequent targets compete spatiotemporally during rapid serial visual processing. We used gaze-contingent eye-tracking to probe the roles of spatiotemporal competition and memory encoding on the spatial distribution of interference caused by emotional distractors, while also ruling out the role of eye-gaze in driving differences in spatial distribution. Spontaneous target perception impairments caused by emotional distractors were localized to the distractor location regardless of where participants fixated. But when emotional distractors were task-relevant, perceptual lapses occurred across both streams while remaining strongest at the distractor location. These results suggest that spatiotemporal competition and memory encoding reflect a dual-route impact of emotional stimuli on target perception during rapid visual processing.     

Transfer of motor learning engages specific neural substrates during motor memory consolidation dependent on the practice structure

The authors investigated how brain activity during motor-memory consolidation contributes to transfer of learning to novel versions of a motor skill following distinct practice structures. They used 1 Hz repetitive Transcranial Magnetic Stimulation (rTMS) immediately after constant or variable practice of an arm movement skill to interfere with primary motor cortex (M1) or dorsolateral prefrontal cortex (DLPFC). The effect of interference was assessed through skill performance on two transfer targets: one within and one outside the range of practiced movement parameters for the variable practice group. For the control (no rTMS) group, variable practice benefited delayed transfer performance more than constant practice. The rTMS effect on delayed transfer performance differed for the two transfer targets. For the within-range target, rTMS interference had no significant affect on the delayed transfer after either practice structure. However, for the outside-range target, rTMS interference to DLPFC but not M1 attenuated delayed transfer benefit following variable practice. Additionally, for the outside-range target, rTMS interference to M1 but not DLPFC attenuated delayed transfer following constant practice. This suggests that variable practice may promote reliance on DLPFC for memory consolidation associated with outside-range transfer of learning, whereas constant practice may promote reliance on M1 for consolidation and long-term transfer.     

Working memory load reduces the late positive potential and this effect is attenuated with increasing anxiety

Emotion regulation decreases the processing of arousing stimuli, as indexed by the late positive potential (LPP), an electrocortical component that varies in amplitude with emotional arousal. Emotion regulation increases activity in the prefrontal areas associated with cognitive control, including the dosolateral prefrontal cortex (DLPFC). The present study manipulated working memory load, known to activate the DLPFC, and recorded the LPP elicited by aversive and neutral IAPS pictures presented during the retention interval. The LPP was larger on low-load compared to high-load trials, and on trials with aversive compared to neutral pictures. These LPP data suggest that emotional content and working memory load have opposing effects on attention to distracting stimuli. State anxiety was associated with reduced modulation of the LPP by working memory load. Results are discussed in terms of competition for attention between emotion and cognition and suggest a relationship between DLPFC activation and the allocation of attentional resources to distracting visual stimuli–a relationship that may be disrupted with increasing anxiety.     

rTMS for PTSD: induced merciful oblivion or elimination of abnormal hypermnesia?

Neuroimaging studies and experimental data suggest that symptoms of posttraumatic stress disorder (PTSD) are associated with dysfunctions of neural circuits linking prefrontal cortex and the limbic system that have a role in autobiographic episodic memory. High-frequency repetitive transcranial magnetic stimulation (rTMS) of the right dorsolateral prefrontal cortex (DLPFC) has been suggested to be beneficial to patients with PTSD, transiently alleviating re-experiencing as well as avoidance reactions and associated anxiety symptoms. In healthy humans, converging evidence suggests that rTMS of the right DLPFC interferes with episodic memory retrieval. Hence, we hypothesize that daily applications of rTMS in PTSD patients may reduce access to the set of autobiographical stored events, that, if re-experienced, may cause the overt PTSD symptoms.     

Emotion-modulated performance and activity in left dorsolateral prefrontal cortex

Functional MRI (fMRI) was used to examine the relationship between processing of pleasant and unpleasant stimuli and activity in prefrontal cortex. Twenty volunteers identified the colors in which pleasant, neutral, and unpleasant words were printed. Pleasant words prompted more activity bilaterally in dorsolateral prefrontal cortex (DLPFC) than did unpleasant words. In addition, pleasant words prompted more activity in left than in right DLPFC. Response speed to pleasant words was correlated with DLPFC activity. These data directly link positive affect, enhanced performance, and prefrontal activity, providing some of the first fMRI evidence supporting models of emotional valence and frontal brain asymmetry based on electroencephalography (EEG).     

无关工作记忆表征的负性情绪信息能否捕获视觉注意?一项眼动研究

研究通过分析视觉搜索任务的首次注视点和行为反应时, 探讨无关工作记忆表征的负性情绪信息对视觉注意选择的影响。实验1发现在反映早期注意选择的首次注视点百分率指标上, 不管工作记忆表征的情绪效价如何, 均出现了显著的注意捕获效应; 实验2发现当采用中性情绪靶子刺激时, 首次注视点百分率指标上仍表现出了稳健的注意捕获效应; 在首次注视点持续时间指标上, 实验1和实验2均发现记忆匹配条件的干扰刺激显著小于控制条件的干扰刺激, 表现出注意的快速脱离; 而在行为反应时指标上, 早期的注意捕获效应消失(实验1), 甚至被反转为注意抑制效应(实验2)。这些结果表明在早期注意选择阶段, 记忆驱动的注意捕获效应不受工作记忆表征情绪效价的影响, 但认知控制会在早期注意捕获之后促使注意快速脱离记忆匹配的干扰刺激, 其作用效果受靶子刺激情绪效价的调节。     

Transfer of Motor Learning Engages Specific Neural Substrates During Motor Memory Consolidation Dependent on the Practice Structure

The authors investigated how brain activity during motor-memory consolidation contributes to transfer of learning to novel versions of a motor skill following distinct practice structures. They used 1 Hz repetitive Transcranial Magnetic Stimulation (rTMS) immediately after constant or variable practice of an arm movement skill to interfere with primary motor cortex (M1) or dorsolateral prefrontal cortex (DLPFC). The effect of interference was assessed through skill performance on two transfer targets: one within and one outside the range of practiced movement parameters for the variable practice group. For the control (no rTMS) group, variable practice benefited delayed transfer performance more than constant practice. The rTMS effect on delayed transfer performance differed for the two transfer targets. For the within-range target, rTMS interference had no significant affect on the delayed transfer after either practice structure. However, for the outside-range target, rTMS interference to DLPFC but not M1 attenuated delayed transfer benefit following variable practice. Additionally, for the outside-range target, rTMS interference to M1 but not DLPFC attenuated delayed transfer following constant practice. This suggests that variable practice may promote reliance on DLPFC for memory consolidation associated with outside-range transfer of learning, whereas constant practice may promote reliance on M1 for consolidation and long-term transfer.     

Repetitive transcranial magnetic stimulation may induce language switching in bilingual patients

The dorsolateral prefrontal cortex (DLPFC) may participate in the process of language switching in multilingual individuals. We present two cases of bilingual patients who experienced unexpected language switching after receiving high-frequency, repetitive transcranial magnetic stimulation (rTMS) to the left DLPFC as a treatment for major depression. These preliminary findings support the role of the DLPFC in language switching in polyglots and highlight the potential value of rTMS for non-invasively investigating language function in humans. Further investigation is warranted.     

When Stronger Knowledge Slows You Down: Semantic Relatedness Predicts Children's Co‐Activation of Related Items in a Visual Search Paradigm

A large literature suggests that the organization of words in semantic memory, reflecting meaningful relations among words and the concepts to which they refer, supports many cognitive processes, including memory encoding and retrieval, word learning, and inferential reasoning. The co‐activation of related items has been proposed as a mechanism by which semantic knowledge influences cognition, and contemporary accounts of semantic knowledge propose that this co‐activation is graded—that it depends on how strongly related the items are in semantic memory. Prior research with adults yielded evidence supporting this prediction; however, there is currently no evidence of graded co‐activation early in development. This study provides the first evidence that in children the co‐activation of related items depends on their relational strength in semantic memory. Participants (N = 84, age range: 3–9 years) were asked to identify a target (e.g., bone) amid distractors. Children's responses were slowed down by the presence of a related distractor (e.g., puppy) relative to unrelated distractors (e.g., flower)—suggesting that children co‐activated related items upon hearing the name of the target. Importantly, the degree of this co‐activation was predicted by the strength of the target–distractor relation, such that distractors more strongly related to the targets slowed down children to a larger extent. These findings have important implications for understanding how organized semantic knowledge affects other cognitive processes across development.     

Goal-relevant events need not be rare to boost memory for concurrent images

In the attentional boost effect, memory for images presented at the same time as unrelated targets (e.g., an orange square) is enhanced relative to images presented at the same time as distractors (e.g., a blue square). One difficulty in understanding the nature of this enhancement is that, in most experiments demonstrating the attentional boost effect, targets have been less common than distractors. As a result, the memory enhancement associated with target detection may have been driven by differences in the relative frequencies of targets and distractors. In four experiments, participants encoded images into memory at the same time that they monitored a second, unrelated stimulus stream for targets. In some conditions, targets were as common as distractors (1:1 ratio); in others, targets were rare (1:6 ratio). The attentional boost effect was present when the target and distractor frequencies were equated, ruling out oddball and distinctiveness effects as explanations. These effects were observed when targets required a buttonpress and when they were covertly counted. Memory enhancements were not observed for images presented at the same time as rare distractor stimuli. We concluded that selectively attending to events that require an overt or covert response enhances the processing of concurrent information.     

Task difficulty and visual similarity increase a distractor's effects on random shapes

Recognition of random shapes followed by a visual distractor is altered by the type of distractor and whether the distractor needs to be attended. Three experiments tested which characteristics modify a visual distractor's effect on random target shapes presented for 75 to 150 msec. Exp. 1 showed that increasing the number of digits to be remembered (1, 3, or 8) increased the effectiveness of digits as distractors. Exeir effect as visual distractors for random target shapes. Random shapes were highly effective as distractors, while pictures of faces or comples colored pictures had a relatively small effect. In Exp. 3 decreasing the presentation time for novel visual distractors decreased recognition of the distractors but not of random target shapes. However, adding a three-digit distractor after the novel visual distractor did decrease recognition of target shapes. Exps. 2 and 3 showed that the order of the recognition tests of the target and distracting stimuli altered target recognition if and only if subjects did know which was to be reported first. These experiments indicate that the effect of a visual distractor depends on both the extent to which it is allotted attention and its visual similarity to the target stimulus.     

Global shape cannot be attended without object identification.

Whether the global shape of objects can be processed without accessing semantic or identity information was tested. Ss judged which of 2 fragmented forms had the same global shape as a reference stimulus. Matching stimuli could be physically identical, semantically related, or unrelated. The reference stimulus and nonmatching (distractor) form could be semantically related or unrelated. Similarity effects in the related condition were unconfounded with matches nameable and nonnameable forms. For nameable forms, related matching forms facilitated performance; a related distractor disrupted performance. Semantic interference was eliminated when nameable distractors were replaced with nonnameable partners; semantic similarity effects on matching were eliminated with a nonnameable reference stimulus and with inverted targets and distractors. Access to information concerning global shape does not normally occur without object identification.     

Data-driven recognition memory: a new technique and some data on age differences

In this study, we investigate the effect on recognition memory of having target and distractor stimuli consisting of different combinations of low-level elements (letters), relative to when targets and distractors consist of combinations of the same elements (nonoverlap and overlap conditions, respectively). It was found that recognition memory was enhanced in the nonoverlap condition, even though subjects reported being unaware of this experimental manipulation. This confirms the importance of perceptually driven processing in the implicit memory component of recognition memory. The extent to which this effect occurs is found to be age dependent, with elderly subjects benefiting more from having targets and distractors consisting of nonoverlapping elements. This is consistent with the notion that elderly subjects show less reliance on item-specific/contextual detail to support recognition memory.     

Repetition and laterality effects on recognition memory for words and pictures*

Recognition memory for a list of words was tested by presenting a series of items with Ss instructed to make positive responses to targets (list items) and negative responses to distractors (nonlist items). The test items were either words or pictures, and they were presented tachistoscopically either to the left or right visual field. The results showed mean response latencies to be generally faster for stimuli presented to the right visual field. Response times were faster for target and distractor stimuli on their second test presentations than on initial tests, but this effect was much larger for targets. Repetitions were shown to decrease the amount of time necessary to execute the stimulus encoding and initial retrieval stages of recognition. This was also true, although to a lesser extent, if different stimulus forms (words or pictures) were used on the two tests. Subsequent recognition stages, including memory search and decision processes. were apparently independent of test stimulus form.     

Trait anxiety and the neural efficiency of manipulation in working memory

The present study investigates the effects of trait anxiety on the neural efficiency of working memory component functions (manipulation vs. maintenance) in the absence of threat-related stimuli. For the manipulation of affectively neutral verbal information held in working memory, high- and low-anxious individuals (N = 46) did not differ in their behavioral performance, yet trait anxiety was positively related to the neural effort expended on task processing, as measured by BOLD signal changes in fMRI. Higher levels of anxiety were associated with stronger activation in two regions implicated in the goal-directed control of attention--that is, right dorsolateral prefrontal cortex (DLPFC) and left inferior frontal sulcus--and with stronger deactivation in a region assigned to the brain's default-mode network--that is, rostral-ventral anterior cingulate cortex. Furthermore, anxiety was associated with a stronger functional coupling of right DLPFC with ventrolateral prefrontal cortex. We interpret our findings as reflecting reduced processing efficiency in high-anxious individuals and point out the need to consider measures of functional integration in addition to measures of regional activation strength when investigating individual differences in neural efficiency. With respect to the functions of working memory, we conclude that anxiety specifically impairs the processing efficiency of (control-demanding) manipulation processes (as opposed to mere maintenance). Notably, this study contributes to an accumulating body of evidence showing that anxiety also affects cognitive processing in the absence of threat-related stimuli.     

Working memory improvement with non-invasive brain stimulation of the dorsolateral prefrontal cortex: A systematic review and meta-analysis

Recent studies have used non-invasive brain stimulation (NIBS) techniques, such as repetitive transcranial magnetic stimulation (rTMS) and transcranial direct current stimulation (tDCS), to increase dorsolateral prefrontal cortex (DLPFC) activity and, consequently, working memory (WM) performance. However, such experiments have yielded mixed results, possibly due to small sample sizes and heterogeneity of outcomes. Therefore, our aim was to perform a systematic review and meta-analyses on NIBS studies assessing the n-back task, which is a reliable index for WM. From the first data available to February 2013, we looked for sham-controlled, randomized studies that used NIBS over the DLPFC using the n-back task in PubMed/MEDLINE and other databases. Twelve studies (describing 33 experiments) matched our eligibility criteria. Active vs. sham NIBS was significantly associated with faster response times (RTs), higher percentage of correct responses and lower percentage of error responses. However, meta-regressions showed that tDCS (vs. rTMS) presented only an improvement in RT, and not in accuracy. This could have occurred in part because almost all tDCS studies employed a crossover design, possibly due to the reliable tDCS blinding. Study design was also associated with no improvement in correct responses in the active vs. sham groups. To conclude, rTMS of the DLPFC significantly improved all measures of WM performance whereas tDCS significantly improved RT, but not the percentage of correct and error responses. Mechanistic insights on the role of DLPFC in WM are further discussed, as well as how NIBS techniques could be used in neuropsychiatric samples presenting WM deficits, such as major depression, dementia and schizophrenia.