1. INTRODUCTION
Semantic memory is relatively preserved with normal cognitive aging but
declines in early stages of Alzheimer’s disease and related dementia
(AD-RD) including mild cognitive impairment (MCI) (Salmon et al., 1999;
Gainotti et al., 2014; Kraut et al., 2006, 2007; Gustavson et al.,
2020). Although cognitively healthy older adults experience some
challenges with word retrieval (e.g., recalling names) and engage
additional neural resources compared to younger controls (Shafto et al.,
2010; Baciu et al., 2016; Haitas et al., 2021), their semantic knowledge
remains intact (Verhaegen & Poncelet, 2013; Nicholas et al., 1985). In
contrast, older adults with MCI and AD-RD have semantic memory deficits
that may go beyond word retrieval issues and can involve degradation of
semantic knowledge (Dudas et al., 2005; Joubert et al., 2021). With
disease progression from MCI to AD-RD, there is more noticeable semantic
memory deterioration (Pelgrim et al., 2021; Aschenbrenner et al., 2015;
Almeida & Radanovic, 2022). The majority of this research has been
conducted using naming tasks (e.g., confrontational naming, verbal
fluency, associations). One of the major challenges in understanding the
nature of alterations in semantic memory in MCI and AD-RD relates to
difficulty in determining whether deterioration is in word retrieval,
accessing semantic memory, or semantic knowledge per se .
A semantic memory task that examines access to semantic knowledge
without requiring overt word retrieval is thus ideal to investigate
changes in semantic memory retrieval associated with normal versus
pathological aging. We designed the Semantic Object Retrieval Task
(SORT), which examines how objects are retrieved via explicit evaluation
of object-associated features (Kraut et al. 2002; Kraut et al., 2006,
2007). In the SORT paradigm, the features (e.g., “humps” and
“desert”) normally facilitate retrieval of an object (e.g.,
“camel”). While participants are not required to overtly recall the
word (e.g., “camel”), they are asked to judge whether the features
bring to mind a particular object by pushing the ‘yes’ or ‘no’ button on
the response box. Our task is distinct from tasks involving semantic
priming, contextual constraints, etc. where participants are asked to
judge semantic relatedness between stimuli or if stimuli share a
category (probed as individual words/pictures or in the context of a
sentence; Kiefer, 2001; Kutas & Federmeier, 2000; Wlotko et al.,2010).
In contrast, we explicitly require participants to judge whether the
stimuli evoke retrieval of a specific object and not just relatedness.
Electroencephalogram (EEG), with its millisecond temporal resolution and
direct measure of post-synaptic neuronal activity, is a useful tool to
study neural dynamics associated with semantic memory (Chiang et al.,
2016, 2020). Previously, on EEG-based semantic object memory retrieval
test (SORT), we observed differences in event-related potentials (ERPs)
between (1) cognitively normal younger and older adults, and (2)
individuals with MCI and cognitively normal older controls. A frontal
ERP between 800-1000 ms differentiated retrieval from non-retrieval
trials in cognitively normal older adults but not in younger adults,
which was posited to relate to a more extensive search during the
non-retrieval trials with aging (Chiang et al., 2014). A similar
fronto-parietal potential between 950-1050 ms differentiated retrieval
from non-retrieval trials in individuals with MCI but not in cognitively
normal age- and education-matched controls (Chiang et al., 2015),
suggesting a differentiation between normal and pathological aging in
semantic search. This fronto-parietal activity was also found to be
correlated with episodic memory performance. Those with worse
performance on the logical memory subtest (immediate and delayed recall)
of Wechsler Memory Scale- Third Edition (Wechsler, 1997) had a delayed
fronto-parietal ERP effect, supporting the value of this task in
differentiating normal and pathological aging. Despite the utility of
ERPs for examining the temporal unfolding of neural activity, non
phase-locked and time-locked activity is treated as noise during
averaging of ERPs and thus information that could provide useful
information about the underlying neurophysiological process is not
included. The current study was motivated by the additional insights
that time-frequency EEG analysis (Roach et al., 2008; Cavanagh & Frank,
2014) may provide about semantic memory related to the SORT task, and
aimed at examining differences in neural dynamics that could inform how
semantic memory functions differ from normal to pathological aging.
Prior EEG studies using time-frequency analysis have suggested
functional roles of low and high beta (12-20 and 20-30 Hz, respectively)
in lexical semantic retrieval (Bakker et al., 2015; Bastiaansen and
Hagoort, 2006; Slotnick et al., 2002; Lewis & Bastiaansen, 2015; Weiss
& Mueller, 2012). While theta (4-8 Hz) and alpha (8-12 Hz) oscillations
have been linked to word or sentence processing (Bakker et al., 2015;
Bastiaansen and Hagoort, 2006; Li & Yang, 2013; Shahin et al., 2009;
Chiang et al., 2016). Also, the slower frequency bands (theta, alpha)
are thought to be associated with domain-general processes such as
cognitive control and attentional demands during semantic processing
(Cavanagh & Frank, 2014; Klimesch, 2012). How these different frequency
bands specifically relate to semantic memory processing is still under
scrutiny; therefore, the current study examined oscillatory dynamics in
all three frequency bands (theta, alpha, high/low beta) during the SORT
task.
The current literature on EEG oscillations related to semantic memory
mostly involves studies on young adults. There are a few EEG studies
examining time-frequency responses directly elicited by semantic tasks
in normal aging or pathological aging (e.g., MCI) (Markiewicz et al.,
2021; Poulisse et al., 2020; Packard et al., 2020; Mazaheri et al.,
2018), and none have compared such effects across normal and
pathological aging. Since there is not sufficient literature to guide an
adequately-informed a priori hypothesis to focus on specific
frequency bands or time frames, we used a data-driven approach based on
permutation tests to examine neural oscillations on the SORT task.
Our goals were to examine (1) normal aging effects by comparing younger
to cognitively normal older adults and (2) pathological aging effects by
comparing cognitively normal older adults to individuals with MCI. Our
general hypothesis was that changes would be observable at the neural
level with no differences in behavioral performance for normal aging
effects. In contrast, we expected changes both in task performance and
neural oscillations in older adults with MCI compared to their age- and
education-matched cognitively normal controls.