A magnetoencephalographic study of brain activity related to recognition memory in healthy young human subjects

doi:10.1016/S0304-3940(99)01001-0

Neuroscience Letters

Volume 280, Issue 1, 11 February 2000, Pages 69-72

https://doi.org/10.1016/S0304-3940(99)01001-0 Get rights and content

Abstract

Neural activity associated with recognition memory was investigated using magnetencephalography (MEG) in healthy young subjects. At sensor sites overlying frontal and temporoparietal cortices, magnetic evoked fields (MEFs) revealed a difference between studied and unstudied stimuli, which onset about 400 ms following stimulus onset and lasted about 600 ms. MEG yielded reliable source information revealing the activity of three independent dipoles, located in the right medial temporal lobe (MTL), the right inferior frontal and the left inferior parietal cortices. Our findings suggest that neural activity underlying recognition memory from both superficial and deep brain structures can be monitored by MEG.

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Acknowledgements

This work is supported by grants from the DFG (He1531/4-1 and 426,C5) to H.J.H. M.D.R. was supported by the Wellcome Trust. We wish to thank Guillén Fernández and Marty Woldorff for detailed comments on earlier versions of the article and instructive discussions about the data.

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Cited by (35)

Spatiotemporal pattern of brain electrical activity related to immediate and delayed episodic memory retrieval
2020, Neurobiology of Learning and Memory
Citation Excerpt :
These findings are consistent with those of some studies that have consistently related the activation of MTL regions, together with parietal regions, to recollection. Specifically, some MEG and ERP/LORETA studies observed recollection-related brain activity in the parahippocampal gyrus (Breier, Simos, Zouridakis, & Papanicolaou, 1998; Dhond, Witzel, Dale, & Halgren, 2005; Tendolkar et al., 2000), in the right inferior parietal lobe (Kim et al., 2009) and in the precuneus (Dhond et al., 2005; Tendolkar et al., 2000). In addition, our results are in line with previous studies that used higher spatial resolution techniques such as fMRI, which have also emphasized the role of the parahippocampal gyrus (Cansino, 2002; Kahn, Davachi, & Wagner, 2004), the inferior parietal lobe (Herron, Henson, & Rugg, 2004; Vilberg & Rugg, 2007; Yonelinas, Otten, Shaw, & Rugg, 2005), as well as other nearby regions such as the precuneus, the posterior cingulate gyrus and the retrosplenial cortex (Donaldson, Wheeler, & Petersen, 2010; Kahn et al., 2004), in the recollection (for a review see, Eichenbaum et al., 2007; Ranganath & Ritchey, 2012; Vilberg & Rugg, 2008).
In the present study we used the event-related brain potentials (ERP) technique and eLORETA (exact low-resolution electromagnetic tomography) method in order to characterize and compare the performance and the spatiotemporal pattern of the brain electrical activity related to the immediate episodic retrieval of information (words) that is being learned relative to delayed episodic retrieval twenty-minutes later. For this purpose, 16 young participants carried out an old/new word recognition task with source memory (word colour). The task included an immediate memory phase (with three study-test blocks) followed (20 min later) by a delayed memory phase with one test block. The behavioural data showed progressive learning and consolidation of the information (old words) during the immediate memory phase. The ERP data to correctly identified old words for which the colour was subsequently recollected (H/H) compared to the correctly rejected new words (CR) showed: (1) a significant more positive-going potential in the 500–675 ms post-stimulus interval (parietal old/new effect, related to recollection), and (2) a more negative-going potential in the 950–1850 ms interval (LPN effect, related to retrieval and post-retrieval processes). The eLORETA data also revealed that the successful recognition of old words (and probably retrieval of their colour) was accompanied by activation of (1) left medial temporal (parahippocampal gyrus) and parietal regions involved in the recollection in both memory phases, and (2) prefrontal regions and the superior temporal gyrus (in the immediate and delayed memory phases respectively) involved in monitoring, evaluating and maintaining the retrieval products. These findings indicate that episodic memory retrieval depends on a network involving medial temporal lobe and frontal, parietal and temporal neocortical structures. That network was involved in immediate and delayed memory retrieval and during the course of memory consolidation, with greater activation of some nodes (mobilization of more processing resources) for the delayed respect to the immediate retrieval condition.
On the sensitivity of event-related fields to recollection and familiarity
2018, Brain and Cognition
Citation Excerpt :
That is the intention of the research described here. This builds on indications of the general sensitivity of MEG measures to memory processes, which has been accomplished via assessment of ERFs (Tendolkar et al., 2000; Walla et al., 1999; Walla, Hufnagl, Lindinger, Deecke, & Lang, 2001; Walla, Hufnagl, Lindinger, Deecke, Imhof, et al., 2001), time-frequency plots (Düzel et al., 2003; Düzel, Habib, Guderian, & Heinze, 2004; Guderian & Düzel, 2005; Neufang, Heinze, & Düzel, 2006), and/or data transformed into source space (Dhond, Witzel, Dale, & Halgren, 2005; Gonsalves, Kahn, Curran, Norman, & Wagner, 2005; Lee, Simos, Sawrie, Martin, & Knowlton, 2005; Seibert, Hagler, & Brewer, 2011). For ERFs, Düzel and colleagues (Düzel, Neufang, & Heinze, 2005) identified three temporally and spatially separable ERF modulations comprising changes in signal strength for items that attracted correct ‘old’ rather than correct ‘new’ judgments.
The sensitivity of event-related potentials (ERPs) to the processes of recollection and familiarity has been explored extensively, and ERPs have been used subsequently to infer the contributions these processes make to memory judgments under a range of different circumstances. It has also been shown that event-related fields (ERFs, the magnetic counterparts of ERPs) are sensitive to memory retrieval processes. The links between ERFs, recollection and familiarity are, however, established only weakly. In this experiment, the sensitivity of ERFs to these processes was investigated in a paradigm used previously with ERPs. An early frontally distributed modulation varied with memory confidence in a way that aligns it with the process of familiarity, while a later parietally distributed modulation tracked subjective claims of recollection in a way that aligns it with this process. These data points strengthen the argument for employing ERFs to assess the contributions these processes can make to memory judgments, as well as for investigating the nature of the processes themselves.
Magnetoencephalographic correlates of processes supporting long-term memory judgments
2009, Brain Research
Citation Excerpt :
While the number of ERF studies of recognition memory is small in comparison to the number of ERP studies, the existing data indicate that ERFs index some retrieval processing operations. Tendolkar et al. (2000) acquired ERFs in a recognition memory paradigm where visually presented words where the study and test stimuli. They identified a parietally distributed old/new effect between 500 and 800 ms. On the basis of the time course of this effect and its scalp distribution, they hypothesised that it was the magnetic homologue of the left-parietal ERP old/new effect and thus indexed recollection.
The sensitivity of event-related fields (ERFs) to memory retrieval processes is not well determined. This stands in sharp contrast to event-related potential (ERP) studies, as ERPs have been employed widely to address questions about the functional architecture supporting memory retrieval. Despite their success in this endeavour, however, the sensitivity of ERPs to one retrieval process—familiarity—is somewhat limited. This experiment was designed to determine the sensitivity of ERFs to familiarity, and thus to examine the functional leverage that is available to investigate item familiarity via magnetic means of indexing retrieval processing in real-time. The analyses of the ERF data focused on old/new effects, which are differences between the neural activities associated with old (previously studied) and new test items that attract correct memory judgments. The ERFs showed a level of sensitivity to changes in item familiarity superior to that reported previously in very similar studies where ERPs were acquired. Moreover, analyses of the ERF data revealed four functionally distinct old/new effects. These findings provide strong incentives for employing ERFs in subsequent studies of human memory retrieval processing operations.
Recognition memory probes affect what is remembered in schizophrenia
2009, Psychiatry Research
Cognitive psychology offers tools to localize the memory processes most vulnerable to disruption in schizophrenia and to identify how patients with schizophrenia best remember. In this research, we used the University of Southern California Repeatable Episodic Memory Test (USC-REMT; Parker, E.S., Landau, S.M., Whipple, S.C., Schwartz, B.L., 2004. Aging, recall, and recognition: A study on the sensitivity of the University of Southern California Repeatable Episodic Memory Test (USC-REMT). Journal of Clinical and Experimental Neuropsychology 26(3), 428–440.) to examine how two different recognition memory probes affect memory performance in patients with schizophrenia and matched controls. Patients with schizophrenia studied equivalent word lists and were tested by yes–no recognition and forced-choice recognition following identical encoding and storage conditions. Compared with controls, patients with schizophrenia were particularly impaired when tested by yes–no recognition relative to forced-choice recognition. Patients had greatest deficits on hits in yes–no recognition but did not exhibit elevated false alarms. The data point to the importance of retrieval processes in schizophrenia, and highlight the need for further research on ways to help patients with schizophrenia access what they have learned.
A complementary analytic approach to examining medial temporal lobe sources using magnetoencephalography
2009, NeuroImage
Neuropsychological and neuroimaging findings reveal that the hippocampus is important for recognition memory. However, it is unclear when and whether the hippocampus contributes differentially to recognition of previously studied items (old) versus novel items (new), or contributes to a general processing requirement that is necessary for recognition of both types of information. To address this issue, we examined the temporal dynamics and spectral frequency underlying hippocampal activity during recognition of old/new complex scenes using magnetoencephalography (MEG). In order to provide converging evidence to existing literature in support of the potential of MEG to localize the hippocampus, we reconstructed brain source activity using the beamformer method and analyzed three types of processing-related signal changes by applying three different analysis methods: (1) Synthetic aperture magnetometry (SAM) revealed event related and non-event-related spectral power changes; (2) Inter-trial coherence (ITC) revealed time-locked changes in neural synchrony; and (3) Event-related SAM (ER-SAM) revealed averaged event-related responses over time. Hippocampal activity was evident for both old and new information within the theta frequency band and during the first 250 ms following stimulus onset. The early onset of hippocampal responses suggests that general comparison processes related to recognition of new/old information may occur obligatorily.
Neural correlates of immediate and delayed word recognition memory: An MEG study
2008, Brain Research
Citation Excerpt :
They insisted that medial temporal and temporoparietal areas are involved in recognition memory. Tendolkar et al. (2000) also found that the old/new effect was associated with activations in the right medial temporal lobe, right inferior frontal and left inferior parietal areas. In addition, Dhond et al. (2005) attempted to spatiotemporally map the cortical activities underlying delayed word repetition and recognition, and observed activations of the lateral prefrontal cortex, anterior temporal and medial parietal regions from 500 ms after stimulus-onset, as well as the ventral occipitotemporal regions from 700 ms after stimulus-onset.
We investigated the neural correlates of immediate and delayed word recognition memory using whole head magnetoencephalography (MEG). Event-related potential (ERP) and event-related field (ERF) were simultaneously recorded from 10 subjects while performing a continuous recognition memory task. Subjects were required to determine whether the word was “new” (never before presented) or “old” (presented previously). Old items were presented either immediately or delayed with five intervening words, and the words presented only once were referred to as new words. The grand average ERP waveform showed that immediate repetition was associated with early P300 and absence of N400, while delayed repetition and new word were associated with late P300 and presence of N400. Three ERF components were observed for immediate repetition, while four components were observed for delayed repetition and new word conditions. M1 and M2 were observed across all stimulus-presentation conditions. M3 with medial temporal generators was observed only in delayed repetition and new word conditions. M4 was observed earlier in the immediate repetition than in the delayed repetition and new-word conditions. For M4 generators, cingulate gyrus activations were observed for all stimulus-presentation conditions. In addition, activations in the medial temporal areas were observed for both repetition conditions. These results suggest that immediate and delayed recognition memory have similar neural networks except for the additional involvement of medial temporal areas in delayed recognition memory. The functional roles of M3 and M4 peaks were discussed in terms of functional significance of N400 and early/late P300 ERP peaks, which correspond to M3 and M4, respectively.

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A magnetoencephalographic study of brain activity related to recognition memory in healthy young human subjects

Abstract

Section snippets

Acknowledgements

Acta Psychol.

Trends Neurosci.

Electroenceph. Clin. Neurophysiol.

Electroenceph. Clin. Neurophysiol.

The CELEX lexical database (CD-ROM). Linguistic Data Consortium

Separate neural bases of two fundamental memory processes in the human medial temporal lobe

Science

Magnetencephalography – theory, instrumentation, and applications to non-invasive studies of signal processing in the human brain

Rev. Mod. Phys.

Brain potentials during memory retrieval provide neurophysiological support for the distinction between conscious recollection and priming

J. Cogn. Neurosci.

The recording and analysis of event-related potentials

Frontal brain potentials during recognition are modulated by requirements to retrieve perceptual detail

Neuron