Simultaneous EEG–fMRI reveals brain networks underlying recognition memory ERP old/new effects

Hoppstädter, Michael; Baeuchl, Christian; Diener, Carsten; Flor, Herta; Meyer, Patric

doi:10.1016/j.neuroimage.2015.05.026

Cited by 70 publications

(64 citation statements)

References 85 publications

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“…Although scalp-recorded event-related potentials (ERPs) demonstrate a differential positivity over left parietal cortex as a function of recognition memory (hits > CRs, ∼400-800 ms postretrieval cue onset) (33), the anatomical source(s) of this parietal "old/new" effect and its relation to the multiple memoryrelated PPC effects observed with fMRI remain unknown. A recent effort to use simultaneous EEG−fMRI to advance understanding of the temporal profile of parietal activity during retrieval did not reveal a link between ERP and fMRI BOLD effects in any lateral parietal region (34). Importantly, the hypothesis that IPS and SPL subserve distinct computations predicts that these subregions will display different temporal response patterns during memory-based decisions; these patterns promise to directly inform hypotheses about their functional roles.…”

Section: Significancementioning

confidence: 99%

Electrocorticography reveals the temporal dynamics of posterior parietal cortical activity during recognition memory decisions

Gonzalez

Hutchinson

Uncapher

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Theories of the neurobiology of episodic memory predominantly focus on the contributions of medial temporal lobe structures, based on extensive lesion, electrophysiological, and imaging evidence. Against this backdrop, functional neuroimaging data have unexpectedly implicated left posterior parietal cortex (PPC) in episodic retrieval, revealing distinct activation patterns in PPC subregions as humans make memory-related decisions. To date, theorizing about the functional contributions of PPC has been hampered by the absence of information about the temporal dynamics of PPC activity as retrieval unfolds. Here, we leveraged electrocorticography to examine the temporal profile of high gamma power (HGP) in dorsal PPC subregions as participants made old/new recognition memory decisions. A double dissociation in memory-related HGP was observed, with activity in left intraparietal sulcus (IPS) and left superior parietal lobule (SPL) differing in time and sign for recognized old items (Hits) and correctly rejected novel items (CRs). Specifically, HGP in left IPS increased for Hits 300-700 ms poststimulus onset, and decayed to baseline ∼200 ms preresponse. By contrast, HGP in left SPL increased for CRs early after stimulus onset (200−300 ms) and late in the memory decision (from 700 ms to response). These memory-related effects were unique to left PPC, as they were not observed in right PPC. Finally, memory-related HGP in left IPS and SPL was sufficiently reliable to enable brain-based decoding of the participant's memory state at the single-trial level, using multivariate pattern classification. Collectively, these data provide insights into left PPC temporal dynamics as humans make recognition memory decisions.intracranial EEG | declarative memory | decision making | multivariate pattern analysis | ECoG T he ability to remember past events-episodic memory-is known to critically depend on medial temporal lobe (MTL) structures (1, 2) and their interaction with prefrontal cortex (3). Neuroimaging studies of humans making memory-based decisions, although advancing understanding of MTL and prefrontal mnemonic function (4-8), consistently and unexpectedly demonstrate that activity in left lateral posterior parietal cortex (PPC) also varies with episodic memory outcomes (9-14). In particular, functional MRI (fMRI) data reveal dissociable effects of memory on activity in left intraparietal sulcus (IPS), superior parietal lobule (SPL), and angular gyrus (AG), wherein activity tracks perceived memory strength, retrieval decision uncertainty, and episodic recollection, respectively (9-14). For example, during recognition memory decisions, activity in left lateral IPS is greater during higher confidence hits and monotonically decreases across lower confidence hits to lower confidence correct rejections (CRs) to higher confidence CRs (15-17). By contrast, activity in left SPL is greater during lower confidence recognition decisions (for both hits and correct rejections) relative to higher confidence decisions (11,16,17).Studies of ...

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Section: Significancementioning

confidence: 99%

Electrocorticography reveals the temporal dynamics of posterior parietal cortical activity during recognition memory decisions

Gonzalez

Hutchinson

Uncapher

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…These findings suggest that aerobic exercise during encoding impaired the recollection processing, whereas the familiarity process remained unaffected. Neuroimaging studies have shown that the hippocampus selectively supports the recollection process, whereas adjacent cortex in the medial temporal lobe supports the familiarity process (Cansino et al, 2002;Hoppstadter et al, 2015;Yonelinas et al, 2005). Thus, the behavioral findings of this study suggest that simultaneous exercise and encoding selectively impairs hippocampal functioning.…”

Section: Discussionmentioning

confidence: 48%

“…However, our results indicated that the parietal old/new effect was found in the exercise condition but absent in the rest condition, which was the opposite of our prediction. Hoppstadter et al (2015) examined brain activations that were associated with the parietal old/new effect using simultaneous EEG-functional magnetic resonance imaging recordings and found a relationship between hippocampal activation and the parietal old/new effect. Therefore, it is likely that the observed parietal old/new effect in the exercise condition were indicative of exercise-induced hippocampal activation.…”

Section: Discussionmentioning

confidence: 99%

“…Therefore, the accuracy of old or new judgments and source accuracy of the source memory task can be used as measures of familiarity and recollection, respectively. Neuroimaging studies have indicated that hippocampus plays a critical role in the recollection process, but not in the familiarity process (Cansino, Maquet, Dolan, & Rugg, 2002;Hoppstadter, Baeuchl, Diener, Flor, & Meyer, 2015;Yonelinas, Otten, Shaw, & Rugg, 2005; see also Eichenbaum, Yonelinas, & Ranganath, 2007;Konkel & Cohen, 2009 for reviews).…”

mentioning

confidence: 99%

“…Wilding (2000) further indicated that an increased number of correct source judgments were associated with increased parietal old/new effect. In addition, a neuroimaging study has suggested that the parietal old/new effect reflects hippocampal activation (Hoppstadter et al, 2015). Collectively, the parietal old/new effect is thought to reflect brain activity involved in the source retrieval process (i.e., recollection) and negative and positive effects of aerobic exercise on the recollection processes would be denoted by a decreased or increased parietal old/new effect, respectively.…”

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confidence: 99%

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Aerobic Exercise During Encoding Impairs Hippocampus-Dependent Memory

Soga

Kamijo

Hayashi³

2017

Journal of Sport and Exercise Psychology

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We investigated how aerobic exercise during encoding affects hippocampus-dependent memory through a source memory task that assessed hippocampus-independent familiarity and hippocampus-dependent recollection processes. Using a within-participants design, young adult participants performed a memory-encoding task while performing a cycling exercise or being seated. The subsequent retrieval phase was conducted while sitting on a chair. We assessed behavioral and event-related brain potential measures of familiarity and recollection processes during the retrieval phase. Results indicated that source accuracy was lower for encoding with exercise than for encoding in the resting condition. Event-related brain potential measures indicated that the parietal old/new effect, which has been linked to recollection processing, was observed in the exercise condition, whereas it was absent in the rest condition, which is indicative of exercise-induced hippocampal activation. These findings suggest that aerobic exercise during encoding impairs hippocampusdependent memory, which may be attributed to inefficient source encoding during aerobic exercise.

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Exploring the Event‐Related Potentials' Time Course of Associative Recognition in Autism

et al. 2020

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Behavioral data on episodic recollection in autism spectrum disorders (ASD) point limited relational memory functioning. However, the involvement of successive memory processes in the profile of episodic memory in ASD needs more study. Here, we used event-related potentials (ERP) to investigate the time course of episodic recollection with an associative recognition paradigm with picture pairs. Twenty-two participants with ASD and 32 with typical development (TD), all right-handed, were included. Behavioral results confirmed difficulties in correctly recognizing identical pairs in the ASD relative to TD group. We found an unexpected amplitude decrement on the P2 (220-270 msec) and FN400 (350-470 msec) potentials, suggesting diminished priming and familiarity effects in the ASD relative to TD group. However, ERP data revealed that the recognition of associative information relies on the same electrophysiological process (old/new effect in the 600-700-msec late positive component) in ASD participants as in TD ones, with a parietal extension in the ASD group. These results suggest that the electrophysiological processes of associative recognition are qualitatively similar in individuals with and without ASD but may differ quantitatively. This difference may be driven by the reduced early processing of picture pairs that may in turn lead to their diminished integration into the semantic memory system, being partially compensated by a greater involvement of associative memory during the recollection process. Other studies would be useful to go further in identifying these cognitive processes involved in atypical recognition in ASD and their neural substrates.

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Simultaneous EEG–fMRI reveals brain networks underlying recognition memory ERP old/new effects

Cited by 70 publications

References 85 publications

Electrocorticography reveals the temporal dynamics of posterior parietal cortical activity during recognition memory decisions

Electrocorticography reveals the temporal dynamics of posterior parietal cortical activity during recognition memory decisions

Aerobic Exercise During Encoding Impairs Hippocampus-Dependent Memory

Exploring the Event‐Related Potentials' Time Course of Associative Recognition in Autism

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