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Inflammation, Anxiety & Memory in Young Adults

This document summarizes a research article that studied the relationship between recognition memory performance and various health factors in young adults. The study measured two components of recognition memory (recollection and familiarity) using an associative recognition task with word pairs. Regression analyses were used to relate recognition memory to physical health measures (inflammation, central obesity, heart rate variability) and mental health measures (depression, stress, anxiety). The analyses found that together these health factors predicted 19% of the variance in recollection and 15% of the variance in familiarity. Inflammation, depression, and trait anxiety each independently predicted recognition memory performance. Higher depression/inflammation were linked to worse recollection but better familiarity, while higher trait anxiety was linked
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0% found this document useful (0 votes)
58 views26 pages

Inflammation, Anxiety & Memory in Young Adults

This document summarizes a research article that studied the relationship between recognition memory performance and various health factors in young adults. The study measured two components of recognition memory (recollection and familiarity) using an associative recognition task with word pairs. Regression analyses were used to relate recognition memory to physical health measures (inflammation, central obesity, heart rate variability) and mental health measures (depression, stress, anxiety). The analyses found that together these health factors predicted 19% of the variance in recollection and 15% of the variance in familiarity. Inflammation, depression, and trait anxiety each independently predicted recognition memory performance. Higher depression/inflammation were linked to worse recollection but better familiarity, while higher trait anxiety was linked
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© © All Rights Reserved
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The Journal of General Psychology

ISSN: (Print) (Online) Journal homepage: https://www.tandfonline.com/loi/vgen20

Inflammation, depression, and anxiety related to


recognition memory in young adults

James D. Schaeffer, Cory Newell, Catherine Spann, George Siemens & Angela
Liegey Dougall

To cite this article: James D. Schaeffer, Cory Newell, Catherine Spann, George Siemens
& Angela Liegey Dougall (2023) Inflammation, depression, and anxiety related to
recognition memory in young adults, The Journal of General Psychology, 150:1, 1-25, DOI:
10.1080/00221309.2021.1893638

To link to this article: https://doi.org/10.1080/00221309.2021.1893638

Published online: 17 Mar 2021.

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https://www.tandfonline.com/action/journalInformation?journalCode=vgen20
THE JOURNAL OF GENERAL PSYCHOLOGY
2023, VOL. 150, NO. 1, 1–25
https://doi.org/10.1080/00221309.2021.1893638

Inflammation, depression, and anxiety related to


recognition memory in young adults
James D. Schaeffera , Cory Newellb,d, Catherine Spannc, George Siemensb,d,
and Angela Liegey Dougallb,d
a
Department of Psychology, Stephen F. Austin State University, Nacogdoches, TX, USA;
b
Department of Psychology, University of Texas at Arlington, Arlington, TX, USA; cInstitute of
Cognitive Science, University of Colorado Boulder, Boulder, CO, USA; dLINK Research Lab,
University of Texas at Arlington, Arlington, TX, USA

ABSTRACT ARTICLE HISTORY


Previous research suggests that common modifiable health risk Received 8 April 2020
factors (e.g., depression, anxiety, metabolic illness, inflammation) Accepted 17 January 2021
may have an impact on memory. In the present study, we
KEYWORDS
sought to investigate relationships between a number of these
Anxiety; depression;
health risk factors and two components of recognition memory familiarity; inflammation;
(recollection and familiarity). Data were analyzed for 96 healthy recollection
young adults between 17 and 25 years old. Recollection and
familiarity were measured using an associative recognition pro-
cedure involving unitized and unrelated word pairs, and regres-
sion analyses were used to relate recognition memory
performance to physical health (inflammation via plasma IL-6
levels, central obesity via waste-to-hip ratio, and heart rate vari-
ability) and mental health (depression via CESD-R, stress via PSS,
and state and personality trait anxiety via STAI) measures of
modifiable risk factors. Together, these health variables predicted
an additional 19% of the variance in recollection beyond what
was accounted for by familiarity, and 15% of the variance in
familiarity beyond what was accounted for by recollection.
These effects were primarily driven by inflammation, depression,
and trait anxiety, which were each significant (p < .05) inde-
pendent predictors of recognition. Higher levels of depression
and inflammation were related to worse recollection yet better
familiarity. Higher levels of trait anxiety were related to better
recollection but were not related to familiarity. These findings
demonstrate complex relationships between these modifiable
health risk factors and recognition memory. Future longitudinal
and cross-sectional research is needed to further explore these
relationships and determine whether or not poor health causes
these changes in recognition.

Introduction
Modifiable and lifestyle-related aspects of health can have an impact on
our neurological processes. Recently, there has been much interest in

CONTACT James D. Schaeffer [email protected] Department of Psychology, Stephen F. Austin State


University, P.O. Box 13046, SFA Station, Nacogdoches, TX 75962, USA.
ß 2021 Taylor & Francis Group, LLC
2 J. D. SCHAEFFER ET AL.

studying psychological and physiological health factors and how they may
relate to memory function. In the present study, we sought to investigate
relationships between some of these health factors and components of rec-
ognition memory, recollection, and familiarity. We chose a wide lens for
the present study and included health factors related to both psychological
and physiological health. A brief overview of some of these health factors
and the ways in which they may relate to recognition memory are dis-
cussed below.

Health factors and memory


A variety of psychological and physiological health factors have been shown
to relate to memory performance. For example, memory deficits in depres-
sion have been documented for decades (Burt, Zembar, & Niederehe, 1995;
Dillon & Pizzagalli, 2018; Rock, Roiser, Riedel, & Blackwell, 2014; van
Vreeswijk & de Wilde, 2004), and evidence also suggests that depression is
a risk factor for the development of dementia later in life (Chan, Yiu,
Kwok, Wong, & Tsoi, 2019; Cherbuin, Kim, & Anstey, 2015; Diniz,
Butters, Albert, Dew, & Reynolds, 2013). Like depression, there is also con-
siderable evidence linking chronic stress to memory dysfunction (Kim &
Diamond, 2002; Sauro, Jorgensen, & Teal Pedlow, 2003), and theoretical
mechanisms linking stress, depression, and memory have now been pro-
posed. Chronically elevated levels of stress hormones, often experienced by
patients with depression, can damage the hippocampus (Dillon &
Pizzagalli, 2018; Kim & Diamond, 2002; McEwen, Nasca, & Gray, 2016), a
brain region crucial for episodic memory. Therefore, chronic stress may be
an underlying mechanism causing both depression and memory deficits.
Many common physiological health factors may also have an impact on
memory. For instance, research has linked symptoms related to the meta-
bolic syndrome, such as obesity and diabetes, to memory dysfunction
(Cardoso & Moreira, 2019; Cheke, Bonnici, Clayton, & Simons, 2017).
Evidence from animal studies has suggested that many of the mechanisms
underlying the link between metabolic dysfunction and memory involve
specific effects on the hippocampus (Abbott et al., 2019; Chesnokova,
Pechnick, & Wawrowsky, 2016; Kanoski & Davidson, 2011). For example,
McNay et al. (2010) showed that high-fat-diet-induced insulin resistance
reduced hippocampal responses to insulin, and that hippocampal insulin
signaling related to hippocampal-dependent memory. Likewise, Beilharz,
Maniam, and Morris (2016) showed that weight gain related to memory
deficits in mice fed high-fat and high-sugar diets, and that these diets
affected inflammatory gene expression in the hippocampus. Interestingly,
they showed that inflammatory gene expression was not significantly
THE JOURNAL OF GENERAL PSYCHOLOGY 3

altered in perirhinal cortex, suggesting that these effects were specific to the
hippocampus. There is also human evidence supporting a link between
inflammation and the hippocampus, as Marsland, Gianaros, Abramowitch,
Manuck, and Hariri (2008) showed a negative relationship between
circulating interleukin 6 levels and hippocampal gray matter volumes in
middle-aged adults. Furthermore, the presence of many of these metabolic
symptoms in midlife has been shown to be predictive of the development
of dementia in later life (Tortelli et al., 2017), suggesting that these factors
may begin to have an impact on brain function early in adulthood.

Recognition memory
In the present study, we chose to investigate relationships between com-
mon modifiable mental and physical health risk factors and recognition
memory performance in young adults. We employed a task designed to
separate subcomponents of recognition memory: recollection and familiar-
ity. According to the dual-process model of recognition, recollection and
familiarity are qualitatively different and rely on different brain regions
(Diana, Yonelinas, & Ranganath, 2007; Eichenbaum, Yonelinas, &
Ranganath, 2007; Montaldi & Mayes, 2010; Ranganath, 2010; Yonelinas,
2002). Recollection refers to recognition that involves the conscious recall
of specific contextual or associated details of an experienced event, whereas
familiarity refers to recognition that involves a strong feeling that a stimu-
lus has been previously encountered without recall of contextual or associ-
ated details of the initial encounter. Considerable support for this model of
recognition memory comes from neuroimaging studies, and although much
research has dissociated recollection from familiarity in medial temporal
lobe structures (Diana et al., 2007; Eichenbaum et al., 2007; Montaldi &
Mayes, 2010; Ranganath, 2010), others have shown that these processes can
be dissociated in many brain regions, including the prefrontal cortex
(Scalici, Caltagirone, & Carlesimo, 2017), parietal cortex (Wagner,
Shannon, Kahn, & Buckner, 2005), the striatum (King, de Chastelaine,
Elward, Wang, & Rugg, 2018), and the thalamus (Carlesimo, Lombardi,
Caltagirone, & Barban, 2015). This evidence suggests that these two recog-
nition processes involve differential neural mechanisms across widespread
brain networks.
Recollection and familiarity are often studied using tests of associative
memory. Some examples of associated stimuli that have been used in previ-
ous studies are face/name pairs, object/background pairs, image/location
pairs, and two-word or two-image pairs (see Mayes, Montaldi, & Migo,
2007 for examples). With all procedures, recognition of an item (e.g., face,
object, image, or word) with its associated pair (e.g., name, background,
4 J. D. SCHAEFFER ET AL.

location, or word) implies recollection-based recognition, whereas recogni-


tion of an item without memory for its associated pair suggests familiarity-
based recognition. Therefore, the key factor that differentiates recollection
from familiarity using these procedures is the formation of new associa-
tions between items or between items and their contexts. Recollection of
these newly formed associations are later assessed using an associative
memory recognition test.
Another approach to investigating recollection and familiarity involves
recognition of unitized items. Unitization refers to associated stimuli that
have been incorporated in some way to form a single (i.e., unitized) item
(Diana, Yonelinas, & Ranganath, 2008). For example, if an item (e.g., a
black silhouette of a car) is presented against a colored (e.g., red) back-
ground, both the item and background color can be recognized together as
a unitized pair if the subject formed a mental representation of the item
and background combined together (e.g., a red silhouette of a car) rather
than the item and background as an association (e.g., a black car against a
red background). Past research has shown that associated items can be
remembered together when unitized using familiarity-based recognition
processes (Delhaye & Bastin, 2018; Diana, Van den Boom, Yonelinas, &
Ranganath, 2011; Diana et al., 2008; Kamp, Bader, & Mecklinger, 2016;
Tibon, Gronau, Scheuplein, Mecklinger, & Levy, 2014). Therefore, by com-
paring recognition memory performance of unitized vs. non-unitized asso-
ciated items, one can dissociate familiarity- from recollection-based
recognition.

Recollection, familiarity, and health


The importance of differentiating recollection from familiarity in recogni-
tion memory research is becoming increasingly apparent, as newer research
has dissociated recollection and familiarity across a variety of factors. For
example, recent research has shown that cortisol differentially affects recol-
lection and familiarity (McCullough, Ritchey, Ranganath, & Yonelinas,
2015; McCullough & Yonelinas, 2013; Wiemers et al., 2019). Similarly, evi-
dence has also shown that recollection deficits are more often observed in
patients with depression than are deficits in familiarity (Dillon & Pizzagalli,
2018; Drakeford et al., 2010; Hertel & Milan, 1994). Likewise, some evi-
dence also suggests that age-related memory decline affects recollection
more adversely than familiarity (Koen & Yonelinas, 2014, 2016). Therefore,
because recognition can be accomplished through either process, measuring
both recollection and familiarity components of recognition memory is cru-
cial for delineating relationships between health factors and recognition
memory. In the present study, we chose to focus on a few modifiable
THE JOURNAL OF GENERAL PSYCHOLOGY 5

mental and physical health risk factors that may relate to memory dysfunc-
tion, including inflammation, visceral obesity, heart rate variability, stress,
anxiety, and depression. These variables may be linked to memory and/or
hippocampal dysfunction either directly or indirectly. For instance, inflam-
mation has been causally linked to hippocampal dysfunction in animal
experiments (Ekdahl, Claasen, Bonde, Kokaia, & Lindvall, 2003; Monje,
Toda, & Palmer, 2003), and other animal research has shown that inflam-
matory mechanisms in the hippocampus influence vulnerability to stress
(Pearson-Leary et al., 2017). There is also human evidence linking
inflammation to the hippocampus, as Marsland et al. (2008) showed that
hippocampal volume correlated with levels of inflammatory cytokines in
middle-aged adults. Similarly, factors linked to heart disease and metabolic
dysfunction have been shown to be related to cognitive dysfunction (Yates,
Sweat, Yau, Turchiano, & Convit, 2012) and an increased risk for the
development of dementia later in life (Razay, Vreugdenhil, & Wilcock,
2007). Likewise, visceral obesity is believed to contribute to chronic inflam-
mation and vascular disease (Mathieu, Poirier, Pibarot, Lemieux, &
Despres, 2009), and some evidence suggests that widespread blood brain
barrier breakdown appears early in the hippocampus and may contribute
to the development of many neurodegenerative diseases (Montagne et al.,
2015; Sweeney, Sagare, & Zlokovic, 2018). Furthermore, psychological
factors, including stress and depression, have been linked to memory
impairment and hippocampal dysfunction (Burt et al., 1995; Kim &
Diamond, 2002; Videbech & Ravnkilde, 2004). And, although the literature
linking trait anxiety to recognition memory has been mixed (for reviews,
see Herrera, Montorio, Cabrera, & Botella, 2017; Mitte, 2008), clear
evidence suggests that chronically elevated levels of stress hormones can
have a negative impact on memory and the hippocampus (Kim &
Diamond, 2002).

The present study


The present study employed an associative memory task involving unitiza-
tion. Studied items were word pairs that were either unrelated (e.g., vol-
cano-hamster) or formed a unitized pair (e.g., paper-towel). This procedure
has been used in previous research to differentiate recollection and famil-
iarity (Ahmad & Hockley, 2014; Zheng, Li, Xiao, Broster, & Jiang, 2015,
2015). Theoretically, participants should be able to recognize unitized pairs
using familiarity-based recognition because there would be no need to
form a new association between them (as one should already exist through
past experience with the English language). However, recognition of unre-
lated pairs would require recollection-based recognition because a new
6 J. D. SCHAEFFER ET AL.

Physical Health
Inflammaon (IL-6)
Recollecon
Visceral Obesity (WHR)
Cardiovascular Fitness (HRV)

Mental Health
Depression (CESD-R)
Stress (PSS)
State Anxiety (STAI)
Trait Anxiety (STAI)
Familiarity
Figure 1. Predicted relationships between the measured health variables and recognition mem-
ory. We hypothesized that all variables would be more strongly related to recollection than
familiarity (depicted as the larger arrow). Higher levels on all variables, except for heart rate
variability, indicate poorer health. Therefore, we expected that all relationships would be nega-
tive, except for heart rate variability. IL-6: Interleukin 6, WHR: waste-to-hip ratio, HRV: heart rate
variability, CESD-R: center for epidemiological studies depression scale-revised, PSS: perceived
stress scale, STAI: state-trait anxiety inventory.

association between them would need to be formed at encoding. Therefore,


by comparing recognition memory performance of unrelated and unitized
word pairs, recollection, and familiarity can be differentiated.
Based on the abovementioned research on health and recognition mem-
ory, we hypothesized that the modifiable health factors measured in the
present study may differentially affect recollection and familiarity.
Specifically, we predicted that poorer health outcomes would more strongly
predict recollection—rather than familiarity—deficits. These predictions
were made based primarily on the potential negative effects that these
measured health variables may have on the hippocampus, as demonstrated
by previous human and animal research. These predictions are depicted in
Figure 1.

Method
Participants
Participants were recruited to take part in a larger study designed to exam-
ine relationships between social media use, health, and cognitive function.
However, the present study did not examine the effects of social media use.
All participants were university students in the United States and were
recruited through the university’s participation recruitment website or
through flyers posted on campus. Participants could earn either a $30 gift
card or credit toward class for participation. Inclusion criteria required par-
ticipants to be healthy, between 17 and 25 years old, and fluent in written
and spoken English. The following were used to exclude unhealthy partici-
pants based on self-report: medication for psychological diagnoses,
THE JOURNAL OF GENERAL PSYCHOLOGY 7

pregnancy, tobacco use, use of anabolic steroids or anti-inflammatory


medication, use of opioids, a recent experience of head trauma (last
6 months) or physical injury, surgery, chemotherapy, or radiation therapy
(last 2 weeks), deafness or tinnitus, seizure disorder, cancer, a history of
significant coronary events, high blood pressure, high cholesterol, diabetes,
hepatitis C or viral cirrhotic hepatic disease, active infection, severe anemia,
connective tissue disease, or any illness not controlled by a stable thera-
peutic regimen. All participants provided their consent to participate, and
all procedures were approved by the University’s Institutional
Review Board.

Procedures
Participants took part in an online and in-lab Phase for this study. The
online phase was used to verify eligibility and captured stable factors of the
individual (e.g., personality). In Phase 2, participants underwent procedures
in the following order, a blood draw, a waist-to-hip ratio measurement,
heart rate data collection during a resting period, completed an associative
memory test on a computer, and completed surveys on a computer
(including those for depression, stress, and anxiety). Participants also com-
pleted a number of surveys that were not part of the present study. Blood
draws occurred between 2:00 p.m. and 4:00 p.m. to reduce variability
attributable to circadian fluctuations in inflammatory marker levels.

Health variables
Waist-to-hip ratio was used to measure visceral obesity, as negative health
outcomes associated with obesity tend to correlate most strongly with fat
accumulation in the viscera compared to other measures of obesity (e.g.,
body mass index, Shuster, Patlas, Pinthus, & Mourtzakis, 2012).
Measurements were taken around the waist between the lowest rib and the
iliac crest and around the hip around the greater trochanters (lateral por-
tion of the top of the femur), as in (Onat et al., 2004). Waist circumference
was divided by hip circumference. Therefore, larger values represented
greater visceral obesity.
Plasma levels of interleukin 6 (IL-6) were used as a measure of inflam-
mation, as high levels of IL-6 have been linked to worse cognitive function-
ing (Wright et al., 2006) and smaller human hippocampal volumes
(Marsland et al., 2008) in humans. Blood samples were collected via veni-
puncture in 10 mL serum separator tubes. Serum was extracted from each
after centrifuge and stored in a 80 C freezer. The sandwich enzyme-
linked immunosorbent assay (ELISA) technique was used to measure IL-6
levels in each sample. These samples were run in duplicate, and average
8 J. D. SCHAEFFER ET AL.

values whose coefficients of variance were below 15% were used in


the analysis.
Electrocardiogram was recorded using the ZephyrTM bioharness, and
these recordings were used to compute HRV. These recordings were made
during a 5-minute rest period prior to completing the memory measures
on the computer, and at least 20 minutes after the blood draw. The root
mean square of the successive differences (RMSSD) of heart beats was used
as a measure of HRV, and was chosen because of its history of use as a
proxy of parasympathetic activity (Laborde, Mosley, & Thayer, 2017).
Kubios software was used to process heart rate data (Tarvainen, Niskanen,
Lipponen, Ranta-Aho, & Karjalainen, 2014).
Self-report scales were used to assess stress, anxiety, and depression
symptoms, and were administered in person using Qualtrics (Qualtirics,
Provo, UT). The following were used: The Perceived Stress Scale (PSS), the
State-Trait Anxiety Inventory (STAI), and the Center for Epidemiological
Studies Depression Scale-Revised (CESD-R). The PSS consisted of 10 items
designed to assess perceived stress over the past month (Cohen, Kamarck,
& Mermelstein, 1983). The STAI consisted of 40 items designed to assess
both state and trait anxiety (Spielberger, Gorsuch, Lushene, Vagg, & Jacobs,
1983). The CESD-R consisted of 20 items designed to assess symptoms of
depression (Eaton, Smith, Ybarra, Muntaner, & Tien, 2004; Van Dam &
Earleywine, 2011). These scales have been widely used and have demon-
strated reliability and validity (Barnes, Harp, & Jung, 2002; Roberti,
Harrington, & Storch, 2006; Van Dam & Earleywine, 2011).

Recognition memory
Recollection and familiarity were assessed by measuring recognition of
unrelated and unitized word pairs, as in Zheng, Li, Xiao, Broster, and Jiang
(2015). With this design, recognition of unrelated pairs is believed to
require recollection, whereas recognition of unitized pairs can be accom-
plished through familiarity, as past research has demonstrated that associ-
ated items can be recognized through familiarity-based recognition if they
had been unitized at encoding (Diana et al., 2008)
Unrelated word pairs were made by pairing two unrelated words (e.g.,
volcano-hamster, toast-pool, mirror-lantern), and unitized word pairs were
made of words that formed a single concept when paired (e.g., fork-lift,
face-mask, side-walk). Rearranged pairs of each type (e.g., from above, for
unrelated: toast-hamster, for unitized: face-lift) were intermixed with old
and new pairs for participants to differentiate during the memory test.
Unitized and unrelated word pairs were taken from previously published
research (Dalton, Tu, Hornberger, Hodges, & Piguet, 2013; Schaeffer et al.,
2014). Because research has shown that recognition of unrelated pairs
THE JOURNAL OF GENERAL PSYCHOLOGY 9

Study TEST
VOLCANO VOLCANO
HAMSTER Unrelated: Intact
HAMSTER
Pleasant Not Pleasant
Intact Rearranged New
2s COB 2s COB
YOLK Unrelated: Rearranged
BOOK
Pleasant Not Pleasant Intact Rearranged New
2s CLOAK 2s TREE
BOOK SEAL
Unrelated: New
Pleasant Not Pleasant Intact Rearranged New
2s CHECK 2s CHECK
MATE Unitized: Intact
MATE
Pleasant Not Pleasant Intact Rearranged New
2s SAND
2s SAND
STORM MAN
Unitized: Rearranged
Pleasant Not Pleasant Intact Rearranged New
2s SNOW 2s MAIN
MAN Unitized: New
FRAME
Pleasant Not Pleasant Intact Rearranged New
2s 2s

Figure 2. Diagram of the experimental paradigm with examples of both unrelated and unit-
ized pairs.

requires recollection, whereas recognition of unitized pairs can be accom-


plished through familiarity (Eichenbaum et al., 2007), this paradigm
allowed us to determine the degree to which each health measure related to
recollection and/or familiarity.
The recognition memory procedure was administered using E-Prime 2.0
(Psychology Software Tools, Pittsburgh, PA). Participants completed a
study phase followed by a recognition test. During study, participants
viewed word pairs on a computer screen, one at a time, and made subject-
ive pleasantness judgments about each pair by responding with either
“pleasant” or “not pleasant” by pressing one of two corresponding keys on
a keyboaFFrd. Each pair remained on screen for 2 seconds. Pleasantness
judgements were not analyzed as part of the experiment, however, as the
purpose of this task was simply to ensure that participants were reading
and paying attention to each word pair. During the recognition test,
studied word pairs were presented again, along with rearranged word pairs
and new word pairs. Studied pairs were presented exactly as they were dur-
ing the study phase, whereas rearranged pairs were presented as rearranged
pairs with other studied words (i.e., words encountered during the study
phase but paired with different studied words to create a different pairing).
New pairs consisted of two entirely new words that were not encountered
during the study phase. Participants responded with either “intact,”
“rearranged,” or “new” by pressing one of three corresponding keys on a
keyboard. During test, word pairs remained on screen for up to 3 seconds
but terminated upon response. This experimental paradigm is depicted in
Figure 2.
During the study, participants encountered 120 word pairs total: 60 unre-
lated and 60 unitized. During the test, participants encountered 120 word
pairs: 20 unrelated-intact, 20 unrelated-rearranged, 20 unrelated-new, 20
unitized-intact, 20 unitized-rearranged, and 20 unitized-new. Word pair
order was randomized for each participant for both the study and the test.
10 J. D. SCHAEFFER ET AL.

Associative memory was assessed by comparing hits (“intact” responses


to intact pairs) to false alarms (“intact” responses to rearranged pairs),
using d’, a measure of discrimination from signal processing theory
(MacMillan & Creelman, 2005). The d’ value was calculated by subtracting
the proportion of false alarms from the proportion of hits using corre-
sponding values from the z-distribution [d’ ¼ z(Hit) – z(False Alarm)]. For
the present study, two d’ values were computed, one for each pair type
(i.e., unrelated and unitized). These values were computed by comparing
the proportion of correct “intact” (i.e., hit) responses to intact pairs relative
to the total number of intact pairs to the proportion of incorrect “intact”
(i.e., false alarm) responses to rearranged pairs relative to the total number
of rearranged pairs. Therefore, with these calculations, d’ represented the
participants’ ability to discriminate studied intact pairs from rearranged
lures for each type of word pair. Recollection was represented as d’ values
for recognition of intact unrelated pairs, and familiarity was represented as
d’ values for recognition of unitized pairs.

Analyses
Data analysis procedures were designed to relate the measured health pre-
dictors to both recollection and familiarity, and all analyses were conducted
using IBM’s SPSS software. First, regression analyses were conducted with
either recollection or familiarity as the criterion, and HRV, WHR, IL-6,
stress (PSS), state anxiety (STAI-state), trait anxiety (STAI-trait), and
depression (CESD-R) as predictors. Gender was also entered as a covariate
because of past evidence of gender differences in many of the included pre-
dictors (Despres & Lemieux, 2006; Keyes, 2004; Regitz-Zagrosek,
Lehmkuhl, & Mahmoodzadeh, 2007). Second, regression analyses were
computed with each type of recognition as criterion, while controlling for
the other using hierarchical regression. For example, with recollection as
the criterion, familiarity was entered into step 1, and health predictors were
entered into step 2. Change in R2 from step 1 to step 2 was interpreted to
assess the unique variance shared between the health variables and each
type of recognition while controlling for the other. These analyses were
designed to allow for the differentiation of recollection and familiarity.
Interpretations of the results were made while taking into consideration
multiple R2, as well as regression coefficients, zero-order correlation coeffi-
cients, and semi-partial correlation coefficients for each predictor variable.
Semi-partial correlation coefficients are displayed in the tables below, as
they represent the proportion of unique variance accounted for by each
predictor when it is included in the model. This allowed us to assess the
relative importance of each individual predictor while accounting for the
THE JOURNAL OF GENERAL PSYCHOLOGY 11

Table 1. Recognition responses for unitized and unrelated word pairs (proportions).
Unitized Word Pairs Unrelated Word Pairs
Rearranged Rearranged
Intact Response Response New Response Intact Response Response New Response
Intact Pair .87 .08 .05 .65 .25 .09
Rearranged Pair .31 .42 .25 .26 .52 .20
New Pair .15 .27 .56 .05 .28 .66
Note. Correct responses were made most often for each pair type.

others. Given the number of predictors, we anticipated having medium to


medium/large effect sizes (Cohen’s f2 between .15 and .25). Power analysis
revealed that between 69 and 109 participants would be needed to detect
these effects with .8 power.

Results
Data
Data were collected from 136 participants. However, data were not avail-
able for all measures for all participants due to a number of reasons out-
lined here: did not complete memory task (n ¼ 2), electrocardiography
recording error/equipment failure (n ¼ 19), did not provide WHR measure-
ments (n ¼ 1), blood serum not obtained (n ¼ 17), unreliable IL-6 from
blood serum (n ¼ 10), did not complete STAI (n ¼ 1). Some participants
had multiple sources of missing data. For all measures (i.e., memory scores,
WHR, PSS scores, STAI State scores, STAI Trait scores, CESD-R scores,
HRV values, and IL-6 levels), full datasets were available for regression
analyses for 96 participants Data distributions were examined for all varia-
bles. CESD-R scores were square root transformed, and STAI State scores,
STAI Trait scores, HRV values, and IL-6 levels were log transformed to
normalize the distributions.

Descriptive statistics and correlations


Table 1 shows response proportions for each pair type. Correct responses
were made most often for each. Survey reliability was assessed
with Cronbach’s alpha, which showed strong internal consistency for all
measures: STAI state (a ¼ .84), STAI trait (a ¼ .91), PSS (a ¼ .83), and
CESD-R (a ¼ .89), Descriptive statistics are presented in Table 2, and the
correlation matrix is presented in Table 3.

Regression analyses
First, the two regression analyses with each type of recognition as criterion
without controlling for the other are presented in Table 4. The regression
12 J. D. SCHAEFFER ET AL.

Table 2. Descriptive statistics for all measures by gender as mean (SD).


All Female (n ¼ 63) Male (n ¼ 33)
WHR 0.82 (0.06) 0.80 (0.05) 0.86 (0.06)
HRV 49.03 (23.68) 47.77 (21.65) 51.45 (27.33)
PSS 17.01 (6.02) 17.94 (5.90) 15.24 (5.93)
STAI Trait 39.44 (9.75) 40.65 (10.43) 37.12 (7.96)
STAI State 34.39 (7.64) 35.46 (8.23) 32.33 (5.94)
CESD-R 10.21 (8.74) 10.92 (9.17) 8.85 (7.82)
IL-6 1.11 (0.82) 1.16 (0.87) 1.01 (0.72)
WHR: waist-to-hip ratio; HRV: Heart Rate Variability; PSS: Perceived Stress Scale; STAI Trait: State-Trait Anxiety
Inventory: Trait Measure; STAIT State: State-Trait Anxiety Inventory: State Measure; CESD-R: Center for
Epidemiological Studies Depression Scale Revised; IL-6: Interleukin 6; HRV: STAI scores, CESD-R scores, and IL-6
levels were transformed for the analyses. Raw scores are presented here.
Variables showing a gender difference, where p < .05

Table 3. Correlation matrix for predictor variables.


Familiarity WHR HRV PSS STAI Trait STAI State CESD-R IL-6
Recollection .51 .04 .07 .17 .28 –.01 .07 .01
Familiarity .23 –.03 .06 .09 –.10 .20 .24
WHR .08 .01 –.03 –.03 .12 .20
HRV –.10 –.10 –.09 .01 .04
PSS .75 .52 .54 .27
STAI Trait .61 .61 .30
STAI State .36 .08
CESD-R .25
WHR: waist-to-hip ratio; HRV: Heart Rate Variability; PSS: Perceived Stress Scale; STAI Trait: State-Trait Anxiety
Inventory: Trait Measure; STAIT State: State-Trait Anxiety Inventory: State Measure; CESD-R: Center for
Epidemiological Studies Depression Scale Revised; IL-6: Interleukin 6.  p < .05

analysis with recollection as the criterion, and gender, PSS, STAI state,
STAI trait, CESD-R, WHR, HRV, and IL-6 as predictor variables was sig-
nificant, R2 ¼ .19, F(8, 87) ¼ 2.58, p ¼ .014. STAI state and STAI trait
were each significant predictors of recollection memory, where higher state
anxiety predicted poorer performance, and higher trait anxiety predicted
better performance. Gender was a marginal predictor, in which being male
predicted poorer performance; no other predictors were significant. The
regression analysis with familiarity as the criterion; and gender, PSS, STAI
state, STAI trait, CESD-R, WHR, HRV, and IL-6 as predictor variables was
only marginally significant, R2 ¼ .14, F(8, 87) ¼ 1.81, p ¼ .086.
Next, the hierarchical regression with recollection as criterion, familiarity
entered into step 1, and gender, PSS, STAI state, STAI trait, CESD-R,
WHR, HRV, and IL-6 entered into step 2 was carried out. The overall
model was significant, R2 ¼ .44, F(9, 86) ¼ 7.55, p < .001. The addition of
step 2 added significant predictive power, DR2 ¼ .19, DF(8, 86) ¼ 3.58,
p ¼ .001, indicating that these health variables significantly predicted recol-
lection above and beyond what was predicted by familiarity. Higher STAI
trait uniquely predicted better recollection, whereas higher IL-6 and CESD-
R scores uniquely predicted poorer recollection. Additionally, higher STAI
state marginally predicted poorer recollection; other predictors were not
significant. Next, a second hierarchical regression was run with familiarity
THE JOURNAL OF GENERAL PSYCHOLOGY 13

Table 4. Unstandardized regression coefficients with standard error, and semi-partial correl-
ation coefficients from the regression analyses.
Criterion Predictors B SE sr
Recollection Gender  –0.28 0.16 –.17
R2 ¼ .19 WHR 1.53 1.33 .11
HRV 0.16 0.14 .11
IL-6 –0.29 0.21 –.13
CESD-R –0.09 0.07 –.14
PSS –0.002 0.02 –.01
STAI State  –0.97 0.39 –.24
STAI Trait  1.71 0.49 .34
Familiarity Gender –0.13 0.21 –.06
R2 ¼ .14 WHR 2.86 1.67 .17
HRV –0.05 0.18 –.03
IL-6 0.37 0.27 .14
CESD-R 0.12 0.08 .15
PSS –0.01 0.02 –.03
STAI State –0.81 0.49 –.16
STAI Trait 0.25 0.61 .04
Recollection Familiarity 0.44 0.07 .50
R2 ¼ .44 Gender –0.22 0.14 –.13
DR2 ¼ .19 WHR 0.27 1.13 .02
HRV 0.19 0.12 .13
IL-6  –0.45 0.18 –.20
CESD-R  –0.14 0.06 –.21
PSS 0.001 0.01 .01
STAI State  –0.61 0.33 –.15
STAI Trait  1.60 0.41 .32
Familiarity Recollection 0.70 0.113 .52
R2 ¼ .41 Gender 0.062 0.175 .03
DR2 ¼ .15 WHR 1.784 1.407 .11
HRV –0.166 0.152 –.09
IL-6  0.576 0.229 .21
CESD-R  0.184 0.069 .22
PSS –0.005 0.018 –.03
STAI State –0.132 0.428 –.03
STAI Trait  –0.95 0.548 –.14
WHR: waist-to-hip ratio; HRV: Heart Rate Variability; PSS: Perceived Stress Scale; STAI Trait: State-Trait Anxiety
Inventory: Trait Measure; STAIT State: State-Trait Anxiety Inventory: State Measure; CESD-R: Center for
Epidemiological Studies Depression Scale Revised; IL-6: Interleukin 6. p < .05,  p < .1

as the criterion, recollection entered into step 1, and gender, PSS, STAI
state, STAI trait, CESD-R, WHR, HRV, and IL-6 entered into step 2. This
overall model was also significant, R2 ¼ .41, F(9, 86) ¼ 6.57, p < .001, and
the addition of step 2 also added significant predictive power, DR2 ¼ .15,
DF(8, 86) ¼ 2.76, p ¼ .009, indicating that these variables also significantly
predicted familiarity above and beyond recollection. Higher IL-6 and
CESD-R scores uniquely predicted greater familiarity, and higher STAI trait
marginally predicted poorer familiarity. Other predictors were not
significant.
Next, because stress and anxiety have sometimes shown quadratic rela-
tionships with cognitive functions in the past (McEwen et al. 2015),
we also re-ran each regression with the addition of quadratic terms for
both PSS an STAI. Quadratic relationships were not observed in
any analysis.
14 J. D. SCHAEFFER ET AL.

Discussion
The purpose of the present study was to investigate relationships between
modifiable health predictors and recognition memory. We had predicted
that health factors would show stronger negative relationships with recol-
lection than with familiarity. The results showed that the hypotheses were
partially supported. When predicting recollection without accounting for
familiarity, state and trait anxiety were each significant predictors. Higher
state anxiety scores were associated with poorer recollection, whereas
higher trait anxiety scores were associated with greater recollection. When
controlling for familiarity, although higher trait anxiety scores still pre-
dicted greater recollection, IL-6 levels and depression scores each became
significant negative predictors of recollection. On the other hand, when
predicting familiarity without controlling for recollection, none of the
health variables were significant predictors. However, when controlling for
recollection, higher inflammation levels and depression scores were related
to greater familiarity. Together, these findings suggested that these modifi-
able health risk factors related to recognition memory in young adults and
that recollection and familiarity may be differentially affected. These data
also supported a dual-process theory of recognition memory (Diana et al.,
2007; Eichenbaum et al., 2007; Montaldi & Mayes, 2010; Ranganath, 2010;
Yonelinas, 2002), which suggested that recollection and familiarity are dif-
ferent and separable processes. Variance in recollection (not accounted for
by familiarity) was accounted for by anxiety scores, depression scores, and
IL-6 levels; variance in familiarity (not accounted for by recollection) was
accounted for by depression scores and IL-6 levels.
The present findings showed that recollection and familiarity may be dif-
ferently influenced by these variables, suggesting that studies using recogni-
tion tests that do not differentiate recollection from familiarity may
produce mixed findings depending on the extent to which each health
measure was represented in their sample and the extent to which the recog-
nition task depended on recollection or familiarity. This is particularly
poignant, as research linking trait anxiety to recognition memory has been
mixed. Two meta-analyses have shown this (Herrera et al., 2017; Mitte,
2008), and the authors of each meta-analysis speculated that one potential
reason underlying mixed findings between recognition and anxiety could
be that the recognition tests used in many of the studies included in the
meta-analyses did not assess recollection. Recent research showing that
acute stress and related cortisol levels can differentially affect recollection
and familiarity (McCullough et al., 2015; McCullough & Yonelinas, 2013)
further supports the need to differentiate recollection and familiarity when
evaluating stress or anxiety effects on recognition memory
THE JOURNAL OF GENERAL PSYCHOLOGY 15

The direction of the relationships between depression scores, trait anxiety


scores, and inflammation with recollection was also noteworthy. Trait anxiety
showed a positive relationship, whereas IL-6 levels and depression scores
showed negative relationships. Although the positive relationship between trait
anxiety and recollection was present with and without the addition of familiar-
ity to the regression model, the negative relationships between IL-6 scores and
depression scores were only present when familiarity was controlled, therefore
supporting the importance of dissociating these components of recognition.
We suggest that these relationships should be interpreted cautiously until
future research is conducted to tease these relationships apart. Nevertheless, a
potential explanation for the direction of these relationships is provided below.
The present findings may be explained by the shared relationships
between the hippocampus and recollection, depression, and inflammation.
Neuroimaging evidence suggests that recollection is dependent on the
hippocampus (Eichenbaum et al., 2007). Evidence also suggests that the
hippocampus may be vulnerable to high levels of inflammation compared
to other brain areas (Freeman, Haley-Zitlin, Stevens, & Granholm, 2011;
Marsland et al., 2008), and others have shown that inflammation can
inhibit hippocampal neurogenesis (Ekdahl et al., 2003; Monje et al., 2003),
suggesting a causal link between inflammation and hippocampal dysfunc-
tion. Similarly, past research has linked depression to memory dysfunction
(Burt et al., 1995) and lower hippocampal volumes (Videbech & Ravnkilde,
2004). Therefore, hippocampal dysfunction may explain these negative rela-
tionships between inflammation and depression and recollection. Future
neuroimaging research is needed, however, to support this interpretation.
Interestingly, positive relationships between IL-6 levels and depression
scores were observed with familiarity, when recollection was controlled.
These patterns may be explained as a shift in recognition memory away
from recollection and toward an increased use of familiarity. This interpret-
ation is partially supported by past research. For example, using a rat
model of recognition memory, Sauvage, Fortin, Owens, Yonelinas, and
Eichenbaum (2008) showed that hippocampal damage resulted in reduced
recollection but increased familiarity. We propose that the psychophysio-
logical mechanisms associated with inflammation and depression may have
inhibited recollection, causing participants with high levels of inflammation
and depression to rely more on familiarity-based recognition in their daily
lives, which could have been reflected in their performance on the recogni-
tion test used in the present study. However, future longitudinal studies
would be needed to support this interpretation.
While the finding that both depression and inflammation were positively
related to trait anxiety was expected, we unexpectedly found that higher
levels of trait anxiety predicted greater recollection. However, it is
16 J. D. SCHAEFFER ET AL.

important to emphasize that past research on the relationship between trait


anxiety and recognition memory has been mixed (Herrera et al., 2017;
Mitte, 2008). Furthermore, although many studies have investigated rela-
tionships between trait anxiety and recognition, we are not aware of any
that have related trait anxiety specifically to recollection and familiarity.
However, a few recent studies have investigated the effects of acute stress
on recollection and familiarity, and each has demonstrated that stress can
differentially impact these two processes (McCullough et al., 2015;
McCullough & Yonelinas, 2013; Wiemers, Hamacher-Dang, Yonelinas, &
Wolf, 2019). Therefore, our results are partially in line with this prior
research, as we too observed differences between recollection and familiar-
ity related to stress, albeit with trait anxiety rather than acute stress.
It is clear that relationships between stress, anxiety, and memory func-
tion are complex (McEwen et al., 2015). However, with this in mind, we
offer the following interpretation to support the present findings. Evidence
has suggested that high anxiety may be associated with a narrowing of the
focus of attention (Harmon-Jones, Gable, & Price, 2013) and hypervigilance
(Richards, Benson, Donnelly, & Hadwin, 2014). Other researchers have sug-
gested that during heightened states of arousal, perceptual competition
leads to better memory for goal-related stimuli (Mather & Sutherland,
2011), and others have shown that norepinephrine, which is released dur-
ing states of high arousal, may be beneficial for hippocampal-dependent
memory (Mather, Clewett, Sakaki, & Harley, 2016). Finally, others have
demonstrated that attention can have a greater impact on recollection than
familiarity (Yonelinas, 2002), an interpretation which is further supported
by research showing that highly arousing stimuli have been shown to be
more likely remembered with recollection than familiarity (Ochsner, 2000).
When considering all of this evidence together with the present research
findings, it may have been the case that participants in the present study
who had reported higher levels of trait anxiety may have been functioning
at a heightened state of arousal during their performance of the memory
task, which may have narrowed their focus of attention to enhance their
memory for unrelated word pairs by increasing hippocampal-dependent
memory via norepinephrine acting on the hippocampus. Furthermore,
given that the memory task required of the participants was not designed
to be particularly stressful, the experience of heightened arousal by partici-
pants with high trait anxiety, may have been within their normal range of
experienced arousal and, therefore, would not have been reported as high
state arousal. This would also explain why state anxiety, unlike trait anxiety,
was not a positive predictor of recollection. We are aware, however, that
this interpretation requires certain assumptions, and we encourage future
investigation of these findings.
THE JOURNAL OF GENERAL PSYCHOLOGY 17

Interestingly, although higher trait anxiety was related to greater recollec-


tion, it was also related to higher levels of inflammation and depression
symptoms. These findings are in line with previous research that has dem-
onstrated negative health effects related to trait anxiety (Michopoulos,
Powers, Gillespie, Ressler, & Jovanovic, 2017; Mineka, Watson, & Clark,
1998). Therefore, although trait anxiety appeared to benefit recollection in
the present study, it may be the case that increases in inflammation and
depression related to anxiety will negate these beneficial effects over time.
Future research on anxiety and recognition memory should take this into
consideration.
A few of the health measures included in the analysis did not predict
recognition. One interpretation for these null findings could be that our
sample consisted of young, healthy adults who have yet to experience the
negative consequences associated with these measures. For example, a
World Health Organization report suggested a cutoff for WHR-related
health risk to be 0.85 for women and 0.90 for men (World Health
Organization, 2011). The range of WHR in our sample was 0.70–0.91 in
females and 0.76–0.95 in males, indicating that only a few individuals met
the criteria for showing unhealthy levels of visceral obesity. This interpret-
ation could also explain why HRV was not a significant predictor of recog-
nition either, although we are not aware of any proposed healthy HRV
recommendations. It may be the case that the physiological states underly-
ing low heart rate variability manifest as significant health problems later
in life, and therefore are not largely apparent in young, relatively healthy
adults. Finally, we also included data from the perceived stress scale in the
hopes that this would provide additional information about the influence
of recent stressful experiences not captured by the STAI. However, the
results of the regression analysis suggested that this measure shared consid-
erable variance with the STAI and was not a uniquely significant predictor
in the final model. Therefore, the PSS may have been a more useful meas-
ure if the STAI were not used.

Limitations
In the present study, measures of recollection and familiarity were highly
correlated. This suggested that these two processes (as measured in the pre-
sent study) were not independent. In the present study, recognition of unit-
ized pairs could have been accomplished through recollection rather than
familiarity, and greater recollection in general may have translated to
greater recollection of both unrelated and unitized word pairs. We
attempted to account for this in our regression analyses by using hierarch-
ical regression and measuring DR2 after controlling for the other
18 J. D. SCHAEFFER ET AL.

recognition component (i.e., controlling for familiarity when predicting rec-


ollection and vice versa). It was only after doing so that inflammation and
depression scores showed significant predictive power. Future research on
these health measures involving different measures of recollection and
familiarity will be needed to provide further support for these findings.
Furthermore, the hypotheses in this study were theoretically based on
models of recognition memory largely involving medial temporal lobe
structures. Primarily, we speculated that, if recollection is hippocampal-
dependent, then health factors that might affect the hippocampus would
impact recollection more greatly than familiarity. However, much
research has demonstrated that recollection- and familiarity-based recog-
nition processing extends well beyond the medial temporal lobes
(Carlesimo et al., 2015; King et al., 2018; Scalici et al., 2017; Wagner
et al., 2005), and because we did not measure the medial temporal lobe
in the present study, we cannot conclude that the observed effects where
the result of the measured health factors having an influence on the
hippocampus. Future neuroimaging research is needed to confirm these
interpretations.

Conclusion
The present study provided evidence that modifiable health variables may
be differentially related to recollection and familiarity in young adults.
Specifically, we showed that higher levels of inflammation and depression
were related to worse recollection yet better familiarity, and that higher lev-
els of trait anxiety were related to better recollection. These findings are
important for a few reasons. First, evidence that health risk factors (i.e., IL-
6, trait anxiety, and depression levels) may have an impact on recognition
memory in young, otherwise healthy adults highlights the importance of
early life interventions for maintaining memory function across the life-
span; these interventions may not be limited to the elderly. Second, they
provide insight into the mixed findings linking trait anxiety to recognition
memory and suggest that this relationship may depend on the extent to
which recognition involves recollection or familiarity. Therefore, future
research in this area should involve recognition memory paradigms that
allow for the dissociation of recollection and familiarity. Finally, these find-
ings suggest complex relationships between depression, inflammation, trait
anxiety, and recognition memory, where trait anxiety may benefit recollec-
tion but may worsen depression and anxiety, each of which may worsen
recollection. Future research is needed in order to tease apart these rela-
tionships and their underlying mechanisms.
THE JOURNAL OF GENERAL PSYCHOLOGY 19

Disclosure statement
No potential conflict of interest was reported by the author(s).

Funding
This research was supported in part by a grant from the National Science Foundation
Grant # 1546393.

Notes on contributors
James Schaeffer, Ph.D. Dr. James Schaeffer studies interactions between memory and cog-
nition, and psychophysiology, neuroscience, and health. Much of his research interests cen-
ter around the ways in which modifiable lifestyle and environmental health factors
throughout lifespan may impact the brain and affect memory. He is an assistant professor
at Stephen F. Austin State University.
Cory Newell, M.S. Cory Newell is a doctoral student in the Department of Psychology at
the University of Texas at Arlington, with a background in health, research design, and sta-
tistics. Broadly, he is interested in the physical and mental health implications of an
increasingly connected and technological society. His current research aims to understand
the impact of increased connectivity by exploring how smartphone and social media use
relate to a variety of health, cognitive, and social factors.
Catherine Spann, Ph.D. Dr. Catherine Spann is a research psychologist specializing in self-
regulation and mindfulness meditation with children and adults. Her current research
examines the effects of breathing practices on stress and emotion regulation. She’s taught
university courses in social, cognitive, and abnormal psychology as well as statistics. She
co-instructs a massive open online course with over 20,000 students called “The Science
and Practice of Yoga.” She is also a certified breath coach and yoga instructor. She is a
post-doctoral researcher at the University of Colorado at Boulder.
Angela Liegey Dougall, Ph.D. Dr. Angela Liegey Dougall has expertise in experimental and
field research using longitudinal, quantitative, and qualitative methods. Her lines of pro-
grammatic research focus on identifying psychological, behavioral, biological, and social
mechanisms and risk factors for outcomes, such as behavior change, academics, and phys-
ical and mental health in numerous populations, including students, student athletes, vic-
tims of traumatic events, and patients with chronic and life-threatening diseases. She is an
associate professor at the University of Texas at Arlington.
George Siemens, Ph.D. Dr. Siemens is an internationally renowned author, researcher, and
theorist in the field of learning, knowledge management, and technology. Prior to his move
to the United States, he was Associate Director of the Technology Enhanced Knowledge
Research Institute (TEKRI) at Athabasca University and Associate Director of Research and
Development at the Learning Technologies Center of the University of Manitoba. He has
organized and presented numerous open online courses, including two entitled
“Connectivism and Connective Knowledge.” He is a highly sought-after consultant and
keynote presenter, having shared his expertise in over 30 countries. Dr. Siemens holds a
doctorate from the University of Aberdeen and a Master of Arts in Distributed Learning
(Leadership and Technology) from Royal Roads University.
20 J. D. SCHAEFFER ET AL.

ORCID
James D. Schaeffer http://orcid.org/0000-0003-0571-9682

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