Age-related ERP differences at retrieval persist despite age-invariant performance and left-frontal negativity during encoding

doi:10.1016/j.neulet.2007.12.016

Neuroscience Letters

Volume 432, Issue 2, 20 February 2008, Pages 151-156

https://doi.org/10.1016/j.neulet.2007.12.016 Get rights and content

Abstract

Although it has been reported repeatedly that retrieval-related processes decline with aging, the influence of well-documented age-related encoding deficiencies on the observed changes at retrieval have not been ruled out as a contributing factor. Here, we disentangle this confound by using a serendipitous finding reported by Nessler et al. [D. Nessler, R. Johnson Jr., M. Bersick, D. Friedman, On why the elderly have normal semantic retrieval but deficient episodic encoding: a study of left inferior frontal ERP activity, Neuroimage 30 (2006) 299–312]. In that study, age-related differences in the magnitude of left inferior frontal brain activity at encoding and subsequent recognition memory performance were eliminated when a deeper level of semantic encoding in the older adults was compared with a shallow level in the young. Based on this earlier result, the present paper is concerned with the question of whether the matched recognition performance resulting from age-equivalent ERP encoding activity was also accompanied by age-invariant retrieval-related brain activity. The results in the young were consistent with dual-process models of recognition memory due to the presence of ERP activity linked previously to familiarity (frontal EM effect) and recollection (parietal EM effect). By contrast the older adults only showed evidence of familiarity-based processes. Thus, despite age-equivalent brain activity at encoding and subsequent recognition performance, older relative to young adults appeared to base their old–new decisions on a qualitatively different pattern of retrieval processes (i.e., more on familiarity and less on recollection). Consequently, these data suggest that the age-related changes in retrieval observed here are independent of, and likely occur in addition to, any age-related changes in encoding processes.

Section snippets

Acknowledgements

We wish to thank Mr. Charles L. Brown III, Ms. Letecia Latif and Ms. Efrat Schori for their invaluable assistance. This research was supported by grant AG05213 from the NIA and by the NYS Department of Mental Hygiene.

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In older adults, true recognition only elicited significant old/new differences at the frontal region during the 400–700 ms time window in the current study. Several previous ERP studies investigating aging effects on old/new effects during memory retrieval have found an age-invariant (e.g., Ally et al., 2008; James, Strunk, Arndt, & Duarte, 2016) or a later onsetting (e.g., Nessler et al., 2007; Nessler et al., 2008) frontal old/new effect in older adults. Therefore, the present frontal old/new effect during a later time window for older adults may suggest that a delayed familiarity process was engaged when correctly recognized the old pictures.
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These results stand in contrast to previous findings showing reduced behavioral estimates of familiarity (Davidson and Glisky, 2002; Duarte et al., 2006; Parks, 2007; Wang et al., 2012a) and attenuated FN400 effects (Duarte et al., 2006; Dulas and Duarte, 2013; Dulas et al., 2011; Trott et al., 1999; Wang et al., 2012a; Wolk et al., 2009) in older adults. However, there is also evidence of age-invariance in the FN400 (Ally et al., 2008; Gutchess et al., 2007; Mark and Rugg, 1998; Nessler et al., 2008; Wegesin et al., 2002). The discrepancies between studies cannot be obviously explained by the presence or absence of group differences in memory accuracy or the procedure used to assess recognition (i.e., remember/know, context memory).
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While aging is associated with a gradual decline in memory, substantial preservation of function is observed in certain individuals and dissecting this heterogeneity is paramount to understanding successful aging. A cohort of elderly individuals were classified according to their level of memory preservation and administered a test of episodic memory in which participants were cued to learn or simply read each word and then to identify previously presented items in a delayed recognition phase. Mathematical modelling revealed that relatively preserved memory function was specifically linked to a faster rate of memorial evidence accumulation (drift rate). Analysis of event-related potentials at encoding revealed that high-performing elderly exhibited signals over parietal regions that discriminated between words to be learned vs. read for an additional 300-ms compared to young subjects suggesting a compensatory encoding mechanism that was absent in the low-performing group. At recognition, parietal signals associated with recollection processes discriminated previously learned words from read words in the young and high-performing old but not in low-performing old. These results reveal that successful aging is associated with specific adaptive neural markers during both encoding and retrieval.
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It has been a controversial issue whether this slowing is generalized or process specific. ERPs have been widely used to study the impact of age on the healthy human brain (Anderer, 2003; Harris et al., 2012; Juckel et al., 2012; Kerr et al., 2010; Nessler et al., 2008; Stothart et al., 2013; Walhovd et al., 2008). Some studies support that stimulus encoding and feature extraction become longer in elderly (Madden and Allen, 1991; Madden, 1988), whereas others suggest that response processes, such as response selection, initiation and execution are slowed (Pratt et al., 1989).
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A critical role of the human hippocampus in an electrophysiological measure of implicit memory
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The hippocampus has traditionally been thought to be critical for conscious explicit memory but not necessary for unconscious implicit memory processing. In a recent study of a group of mild amnesia patients with evidence of MTL damage limited to the hippocampus, subjects were tested on a direct test of item recognition confidence while electroencephalogram (EEG) was acquired, and revealed intact measures of explicit memory from 400 to 600 ms (mid-frontal old–new effect, FN400). The current investigation re-analyzed this data to study event-related potentials (ERPs) of implicit memory, using a recently developed procedure that eliminated declarative memory differences. Prior ERP findings from this technique were first replicated in two independent matched control groups, which exhibited reliable implicit memory effects in posterior scalp regions from 400 to 600 ms, which were topographically dissociated from the explicit memory effects of familiarity. However, patients were found to be dramatically impaired in implicit memory effects relative to control subjects, as quantified by a reliable condition × group interaction. Several control analyses were conducted to consider alternative factors that could account for the results, including outliers, sample size, age, or contamination by explicit memory, and each of these factors was systematically ruled out. Results suggest that the hippocampus plays a fundamental role in aspects of memory processing that are beyond conscious awareness. The current findings therefore indicate that both memory systems of implicit and explicit memory may rely upon the same neural structures – but function in different physiological ways.

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Age-related ERP differences at retrieval persist despite age-invariant performance and left-frontal negativity during encoding

Abstract

Section snippets

Acknowledgements

Acta Psychol.

J. Mem. Lang.

Int. J. Psychophysiol.

Brain Res. Cogn. Brain Res.

Electroencephalogr. Clin. Neurophysiol.

Neuroimage

Brain Res. Cogn. Brain Res.

Trends Cogn. Sci.

Brain Res.

Brain Res. Cogn. Brain Res.

J. Mem. Lang.

Memory changes in healthy older adults

The contribution of recollection and familiarity to recognition memory: a study of the effects of test format and aging

Neuropsychology

Effects of healthy aging on hippocampal and rhinal memory functions: an event-related fMRI study

Cereb. Cortex

Event-related potential (ERP) studies of memory encoding and retrieval: a selective review

Microsc. Res. Tech.

The effects of age on the neural correlates of episodic encoding

Cereb. Cortex

On the neural generators of the P300: evidence from temporal lobectomy patients

Levels of processing effects on memory encoding and retrieval: an ERP Mapping Study

Psychophysiology