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Original Research:
Hippocampal-occipital connectivity reflects autobiographical memory deficits
in aphantasia
Merlin Monzel1,2,*, Pitshaporn Leelaarporn2,3,*, Teresa Lutz2, Johannes Schultz4,5, Sascha
Brunheim3, Martin Reuter1, and Cornelia McCormick2,3
*Both authors contributed equally.
1. Department of Psychology, University of Bonn, 53113 Bonn, Germany
2. German Center for Neurodegenerative Diseases, 53127 Bonn, Germany
3. Department of Neurodegenerative Diseases and Geriatric Psychiatry, University of Bonn
Medical Center, 53127 Bonn, Germany
4. Center for Economics and Neuroscience, University of Bonn, 53113 Bonn, Germany
5. Institute of Experimental Epileptology and Cognition Research, Medical Faculty, University
of Bonn, 53127 Bonn, Germany
Corresponding authors: Cornelia McCormick (cornelia.mccormick@dzne.de), Merlin Monzel
(merlin.monzel@uni-bonn-diff.de)
Number of pages: 43 Number of figures: 3 Number of Tables: 1
Words (abstract): 233 Words (introduction): 647 Words: (discussion): 1441
Conflict of interest statement:
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The authors declare no competing financial interest.
Acknowledgments
C.M. was supported by the German Research Foundation (DFG, MC244/3-1) and the DZNE
Foundation (DZNE Stiftung-Forschung für ein Leben ohne Demenz, Parkinson & ALS). We thank
Anke Rühling and Jennifer Schlee for their technical support during scanning and Yilmaz Sagik
for serving as the secondary AMI scorer. In addition, we would like to thank all participants for
their time and effort to share their memories with us.
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Abstract
Aphantasia prohibits people from experiencing visual imagery. While most of us can readily
recall decade-old personal experiences (autobiographical memories, AM) with vivid mental
images, there is a dearth of information about whether the loss of visual imagery in aphantasics
affects their AM retrieval. The hippocampus is thought to be a crucial hub in a brain-wide
network underlying AM. One important question is whether this network, especially the
connectivity of the hippocampus, is altered in aphantasia. In the current study, we tested 14
congenital aphantasics and 16 demographically matched controls in an AM fMRI task to
investigate how key brain regions (i.e., vmPFC, hippocampus and visual-perceptual cortices)
interact with each other during AM re-experiencing. All participants were interviewed with an
Autobiographical Memory Interview to examine their episodic and semantic recall of specific
events. Aphantasics reported more difficulties in recalling AM, were less confident about their
memories, and described less internal and emotional details than controls. Neurally,
aphantasics displayed decreased hippocampal and increased visual-perceptual cortex activation
during AM retrieval compared to controls. In addition, aphantasics exhibited stronger
connectivity between the hippocampus and the visual cortex during AM and at rest.
Connectivity at rest showed opposite relations to visualization self-reports in the two
participant groups. Our results indicate that visual mental imagery is essential for detailed-rich,
vivid AM and that the functional connection between the hippocampus and visual-perceptual
cortex is crucial for this type of retrieval.
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Keywords: autobiographical retrieval, episodic memory, visual cortex, neural networks,
functional connectivity
Significance Statement
The current study unravels the role of visual mental imagery in episodic autobiographical
memory (AM) retrieval. We show that a lack of mental imagery (= aphantasia) leads to less
detailed memories. Neurally, this deficit is associated with hypoactivity in the hippocampus and
hyperactivity in the visual-perceptual cortices, as well as hyperconnectivity between both
structures. Future studies will show whether mental imagery training leads to changes in these
structures and improves recall of AM, which in turn could be used in various disorders involving
AM deficits such as dementia.
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Introduction
Our unique and personal memories are stored in autobiographical memories (AM) providing
stability and continuity of our self (Svoboda et al., 2006). For most of us, travelling mentally
back in time and re-visiting such unique personal events is associated with vivid, detail-rich
mental imagery (D’Argembeau & Van der Linden, 2006; Greenberg & Knowlton, 2014). This
vivid mental imagery during the re-experiencing of AMs has become a hallmark of autonoetic,
episodic AM retrieval. However, up to date, it remains unclear to what extent episodic AM
retrieval depends on visual mental imagery and what neural consequences a lack of mental
imagery has on episodic AM retrieval. This knowledge gap exists because separating AM
retrieval from mental imagery is a complex and challenging task.
One way to address this conundrum is to study people with aphantasia (Zeman et al.,
2015). Recent research defines aphantasia as a neuropsychological condition in which people
experience a marked reduction or complete lack of voluntary sensory imagery (Monzel et al.,
2022). This condition is associated with psychophysiological alterations, such as reduced
imagery-induced pupil contraction (Kay et al., 2022) and reduced imagery-induced priming
effects (Keogh & Pearson, 2018; Monzel, Keidel, et al., 2021). Thus, aphantasics offer the
unique opportunity to examine the consequences for episodic AM retrieval in the absence of
voluntary imagery. Indeed, a handful of previous studies report convergent evidence that
aphantasics report less sensory AM details than controls (Dawes et al., 2020, 2022; Milton et
al., 2020; Zeman et al., 2020).
Neurally, the hippocampus has been established as a central brain structure to support
the detail-rich episodic AM retrieval in the healthy brain (Bauer et al., 2017; Brown et al., 2018;
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Burianova et al., 2010; McCormick et al., 2020; Moscovitch et al., 2005). In fact, hippocampal
activity correlates with the vividness of AM recollection (Addis et al., 2004; Sheldon & Levine,
2013) and patients with hippocampal damage show marked deficits in retrieving episodic AM
(Miller et al., 2020; Rosenbaum et al., 2008). In addition, neuroimaging studies illuminate that
the hippocampus is almost always co-activated with a wider set of brain regions, including the
ventromedial prefrontal cortex (vmPFC), lateral and medial parietal cortices, as well as visual-
perceptual cortices (Svoboda et al., 2006). Interestingly, especially during the elaboration phase
of AM retrieval, the hippocampus exhibits a strong functional connection to the visual-
perceptual cortices, suggesting a crucial role of this connection for the embedding of visual-
perceptual details into AMs (McCormick et al., 2015).
Yet, not many studies have examined the neural correlates of aphantasia, and none
during AM retrieval. Of the little evidence there is, reports converge on a potential
hyperactivity of the visual-perceptual cortices in aphantasia (Fulford et al., 2018; Keogh et al.,
2020). A prominent theory posits that because of this hyperactivity, small signals elicited during
the construction of mental imagery may not be detected. If true, episodic AM retrieval deficits
seen in aphantasia may be due to a disrupted connectivity between hippocampus and visual-
perceptual cortices (Pearson, 2019). In the same vein, Blomkvist (2022) proposes the extended
constructive episodic simulation hypotheses (CESH+) that suggests that imagination and
memory rely on similar neural structures, since both represent simulated recombinations of
previous impressions. This hypothesis has been supported by shared representations for
memory and mental imagery in early visual cortex (Albers et al., 2013; see also Zeidman &
Maguire, 2016). Within this framework, the hippocampus is supposed to initiate downstream
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sensory retrieval processes (e.g., in the visual-perceptual cortices; Danker & Anderson, 2010),
comparable to its role in the hippocampal memory indexing theory (Langille & Gallistel, 2020; .
Blomkvist (2022) speculates that in aphantasics, either the hippocampal memory index or the
downstream retrieval processes may be impaired.
The main goal of our study was to examine the neural correlates of AM deficits associated
with aphantasia. We hypothesized that the deficits in AM seen in aphantasia rely on altered
involvement of the hippocampus, visual-perceptual cortices and their functional connectivity.
Materials and methods
Participants
In total, 31 healthy individuals with no previous psychiatric or neurological condition
participated in this study. 15 congenital aphantasics and 16 matched controls were recruited
from the database of the Aphantasia Research Project Bonn (Monzel, Keidel, et al., 2021;
Monzel, Vetterlein, et al., 2021). Due to technical issues during MRI scanning, one aphantasic
had to be excluded from the analyses. Groups were matched for basic demographic data, that
is, sex, age, and education, as well as intelligence assessed with a short intelligence screening
(Baudson & Preckel, 2015) (see Table 1). Oral and written informed consent was obtained from
all participants prior to the commencement of experimental procedure in accordance with the
Declaration of Helsinki (World Medical Association, 2013) and the ethics board of the
University Hospital Bonn.
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Table 1.
Demographic data for aphantasics, controls and the total sample.
Total
(n = 30)
Aphantasics
(n = 14)
Controls
(n = 16)
Test
statistic
p
BF01
Age
0.80a
.431
2.30
M
29.77
31.47
28.19
SD
11.36
10.45
12.27
IQ
M
93.77
91.73
95.69
0.81a
.425
2.29
SD
13.53
16.61
10.02
Sex
2.76b
.097
0.69
Male (%)
32.3
53.3
81.3
Female
(%)
67.7
46.7
18.8
Education
1.59b
.662
7.90
Secondar
y school (%)
6.5
6.7
6.3
A-levels
(%)
35.5
40.0
31.3
University
degree
(%)
54.8
46.7
62.5
Doctoral
degree
(%)
3.2
6.7
0.0
Note. BF01 = Bayes Factor, indicates how much more likely H0 is compared to H1. a t-test, b χ2-test.
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Material
Vividness of visual imagery questionnaire
Aphantasia is typically assessed with the Vividness of Visual Imagery Questionnaire (VVIQ;
Marks, 1973, 1995), a subjective self-report questionnaire that measures how vivid mental
scenes can be constructed by an individual. For example, individuals are asked to visualize a
sunset with as much detail as possible and rate their mental scene based on a 5-point Likert
scale (ranging from ‘no image at all, you only “know” that you are thinking of the object’ to
‘perfectly clear and as vivid as normal vision’). Since there are 16 items, the highest score of the
VVIQ is 80 indicating the ability to visualize mental images with such vividness as if the event
were happening right there and then. The minimum number of points is 16 indicating that an
individual reported no mental image for any of the items at all. Aphantasia is at the lower end
of the spectrum of imagery-abilities and usually diagnosed with a VVIQ-score between 16 and
32 (e.g., Dawes et al., 2020, 2022).
Binocular rivalry task
Since self-report questionnaires such as the VVIQ are associated with several drawbacks, such
as their reliance on introspection (Schwitzgebel, 2002), we administered a mental imagery
priming-based binocular rivalry task to assess mental imagery more objectively (for more
details, see Keogh & Pearson, 2018; Pearson et al., 2008). In short, after imagining either red-
horizontal or blue-vertical Gabor patterns, participants were presented with a red-horizontal
Gabor pattern to one eye and a blue-vertical Gabor pattern to the other eye. Subsequently,
participants were asked to indicate which type of Gabor pattern they predominantly observed.
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Usually, successful mental imagery leads subjects to select the Gabor pattern which they had
just visualized. This selection bias can be transferred into a priming score representing visual
imagery strength. Mock stimuli consisting of only red-horizontal or blue-vertical Gabor patterns
were displayed in 12.5 % of the trials to be able to detect decisional biases.
Autobiographical memory interview
Detailed behavioral AM measures were obtained in blinded semi-structured interviews either
in-person or online via Zoom (Zoom Video Communications Inc., 2016) using the
Autobiographical Memory Interview (AMI; Levine et al., 2002). During the AMI, the interviewer
asks the participant to recall five episodic AMs from different life periods: early childhood (up
to age 11), adolescent years (ages 11–17), early adulthood (ages 18–35), middle age (35–55),
and the previous year. For participants who were younger than 34 years, the middle age
memory was replaced by another early adulthood memory. Memories from the first four
periods were considered remote, whereas the memory from the previous year was considered
recent. The interview is structured so that each memory recollection consists of three parts:
free recall, general probe, and specific probe. During free recall, the participants were asked to
recall as many details as possible for a memory of their choice that is specific in time and place
within the given time period. When the participant came to a natural ending, the free recall was
followed by the general and specific probes. During the general probe, the interviewer asked
the participant encouragingly to promote any additional details. During the specific probe,
specific questions were asked for details about the time, place, perception, and
emotion/thoughts of each memory. Then, participants were instructed to rate their recall in
terms of their ability to visualize the event on a 6-point Likert scale (ranging from 'not at all' to
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'very much'). The interview was audiotaped, and afterwards transcribed and then scored by
two independent raters according to the standard protocol (Levine et al., 2002). The interviews
were scored after all data had been collected, in random order, and scorers were blind to the
group membership of the participant.
For scoring, the memory details were assigned to two broad categories, that is, internal
and external details. There were the following subcategories of internal details: internal events
(happenings, weather conditions, people present, actions), place (country, city, building, part of
room), time (year, month, day, time of the day), perceptual details (visual, auditory, gustatory,
tactile, smell, body position), and emotion/thought (emotional state, thoughts). The
subcategories for external details were semantic details (factual or general knowledge),
external events (other specific events in time and place but different to the main event),
repetition (repeated identical information without request), and other details (metacognitive
statements, editorializing). In addition, following the standard procedure, an “episodic
richness” score was given for each memory by the rater on a 7-point Likert scale (ranging from
“not at all” to “perfect”). Furthermore, we added a novel rating score of confidence to the
protocol since many participants indicated very strong belief in the details they provided, while
others were insecure about the correctness of their own memories. Confidence scores were
again rated on a 7-point Likert scale (ranging from 'not at all' to 'perfect').
Experimental design
Experimental fMRI task
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The experimental fMRI task was adapted from a previous protocol by McCormick et al. (2015).
Two conditions, an AM retrieval task and a simple math task (MA), each consisting of 20
randomized trials, were included in this experiment. During AM trials, cue words, such as 'a
party', were presented and participants were instructed to recall a personal event relevant to
the word cue which was specific in time and place (e.g., their 30th birthday party). Participants
were asked to press a response button, once an AM was retrieved to indicate the time point by
which they would start to engage in the AM elaboration phase. For the rest of the trial
duration, participants were asked to re-experience the chosen AM and elaborate as many
details as possible in their mind's eye. After each AM trial, participants were instructed to rate
via button presses whether their retrieval had been vivid or faint. During MA trials, simple
addition or subtraction problems, for example, 47 + 19, were presented. Here, participants
were instructed to press a response button once the problems were solved and asked to
engage in adding 3s to the solutions, for example, (47 + 19) + 3 + ... + 3, until the trial ended.
The MA trials were followed by a rating whether the MA problems had been easy or difficult to
solve. Each trial lasted for a maximum of 17 s and was followed by a jittered inter-stimulus
interval (ISI) between 1 to 4 s.
MRI data acquisition
Anatomical and functional data were acquired at the German Center for Neurodegenerative
Diseases (DZNE), Bonn, Germany, using a 3 Tesla MAGNETOM Skyra MRI scanner (Siemens
Healthineers, Erlangen, Germany). A mirror was mounted on the 32 channel receiver head coil
and was placed in the scanner for the participants to view the stimuli shown on an MRI
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conditional 30-inch TFT monitor (medres medical research, Cologne, Germany) placed at the
scanner’s rear end. The MRI protocol consisted of anatomical, resting-state, and AM task-based
fMRI scanning sessions. Of note, the resting state scans were acquired before participants
engaged in the AM task in order to prevent reminiscing about personal memories during the
resting state. For the anatomical scans, an in-house developed 0.8 mm isotropic whole-brain
T1-weighted sagittal oriented multi-echo magnetization prepared rapid acquisition gradient
echo (MEMPRAGE; Brenner et al., 2014) was employed with the following parameters: TR =
2.56 s, TEs = 1.72/3.44/5.16/6.88 ms, TA = 6:48, matrix = 320 x 320 x 224, readout pixel
bandwidth = 680 Hz/Pixel, CAIPIRINHA mode. Resting-state (190 volumes, TA = 7 min) and AM
task-based fMRI scans (460 volumes, TA = 15 min) were acquired using an interleaved multi-
slice 3.5 mm isotropic echo planar imaging (EPI) sequence with TR = 2 s, TE = 30 ms, matrix = 64
x 64 x 39, readout pixel bandwidth = 2112 Hz/Pixel (see Jessen et al., 2018). The images were
obtained in an oblique-axial slice orientation along the anterior-posterior commissure line.
During resting state, the participants were asked to close their eyes to provoke spontaneous
imagery. The first 5 frames of each functional session were excluded for the scanner to reach
equilibrium. Before each functional session an optimal B0 shim was determined and individually
mapped by 2-echo gradient echo (GRE) with same voxel resolution and positioning for later
post-processing. Additional experimental data were also collected, albeit not part of the current
study.
MRI data processing
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SPM12 (Statistical Parametric Mapping 12) software package (www.fil.ion.ucl.ac.uk/spm/) on
MATLAB v19a (MathWorks) computing platform (https://matlab.mathworks.com/) was used to
perform resting-state and AM task-based fMRI data preprocessing. The anatomical T1w RMS of
all MEMPRAGE’s echoes and functional 2D-EPI images were reoriented along the anterior-
posterior commissure axis. The phase and magnitude images within the field maps were
applied to calculate the voxel displacement maps (VDM) for geometrical correction of the
distorted EPI images. The echo times were set to 4.92 ms (short) and 7.38 ms (long). The total
EPI readout time was 34.56 ms. The calculated EPI and VDMs were applied to the functional
scans for realignment and unwarping. The functional scans were then co-registered to the
segmented bias corrected T1 scans.
Whole-brain differences between groups were evaluated. Thus, co-registered scans were
normalized to the Montreal Neurological Institute (MNI) space and a Gaussian smoothing
kernel of 8 mm FWHM was applied. In addition, for functional connectivity analyses, denoising
was applied using a linear regression model of potential confounding effects (global white
matter signal, CSF signal, and ART scrubbing parameters) in the BOLD signal using CONN
software package (www.nitrc.org/projects/conn/). Temporal band pass filter was set from 0.01
to infinite to further minimize artifacts.
Statistical analyses
Behavioral analyses
Independent samples t-tests were calculated to assess differences in the priming scores of
aphantasics and controls in the binocular rivalry task. One sample t-tests were used to
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distinguish the performances of both groups from chance. To assess differences of AMI scores
between aphantasics and controls, two 2-way mixed ANOVAs with Tukey's multiple comparison
post-hoc tests were calculated, one for internal and one for external memories, with memory
recency (remote vs. recent) as within-subject factor and group (aphantasics vs. controls) as
between-subject factor. Afterwards, two 2-way mixed ANOVAs with Tukey's multiple
comparison were conducted for specific internal (time, place, internal event, perception,
emotion) and external (external event, semantic, repetition, other) memory subcategories.
Differences in memory ratings (confidence, episodic richness) and self-reported visualization
were assessed via t-tests.
Whole-brain fMRI activation analyses
We followed a standard GLM procedure in SPM12 to examine whole-brain activation
differences during AM retrieval and MA between aphantasics and controls. We specified our
main contrast of interest, i.e., AM versus MA on the first level, which was then brought to the
second group level using a two-sided Student t-test. Finally, the activation maps of the two
groups were compared using a two-sample t-test. For whole-brain analysis, we applied a
significance threshold of p < .001, and voxel cluster size of 10 adjacent voxels, uncorrected.
ROI-to-ROI functional connectivity analyses
One of our main hypotheses stated that the hippocampus and visual-perceptual cortex show
differential engagement during AM retrieval associated with aphantasia. Because of the striking
activation differences during AM retrieval between aphantasics and controls in exactly those
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regions, in a next step, we sought to examine the functional connectivity between those areas.
Towards this end, we created regions of interest (ROIs, spheres with a diameter of 10 mm
consisting of 536 voxels) around the three peaks of the activation differences using the
MarsBaR HBM toolbox (Brett et al., 2002). The ROIs comprised (1) the right hippocampus, MNI:
x = 39, y = -31, z = -13, (2) the right visual cortex, MNI: x = 12, y = -79, z = 5, and (3) the left
visual cortex, MNI: x = -9, y = -76, z = 29. Using CONN, we examined functional connectivity (i.e.,
Generalized Psycho-Physiological Interactions, weighted general linear model with bivariate
correlation) between the hippocampal ROI and the ROIs situated in the visual-perceptual cortex
during AM task-based fMRI and during resting-state. Furthermore, in order to examine how
well functional connectivity between hippocampus and the visual cortex reflected an
individuals’ ability to visualize mental events, we examined a regression model with the
visualization scores of the AMI as criterion and connectivity values, group allocation and the
interaction term of connectivity values and group allocation as predictors. For these ROI
analyses, we applied a significance threshold of α = .05, small volume corrected, and a voxel
cluster threshold of 10 adjacent voxels.
Results
Group validation
Aphantasics (M = 16.57, SD = 1.02), scored significantly lower on the VVIQ than controls (M =
62.94, SD = 8.71), t(15.47) = 21.12, p < .001, d = 7.23. Furthermore, aphantasics and controls
differed in the priming score of the binocular rivalry task, t(18.04) = 2.41, p = .027, d = 0.87).
While controls were primed by their own mental imagery in 61.3 % (SD = 13.1 %) of the trials,
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aphantasics were only primed 52.6 % (SD = 4.9 %) of the time. In fact, the performance of
controls differed from chance, t(14) = 3.34, p = .005, d = 0.86, whereas performance of
aphantasics did not, t(13) = 1.96, p = .072. Moreover, the VVIQ scores correlated positively with
the performance on the binocular rivalry task, r(28) = .43, p = .022. For the mock trials, no
differences in priming scores were found between groups, t(28) = 0.86, p = .396, or related to
chance (aphantasics: t(13) = 0.74, p = .475; controls: t(15) = 0.42, p = .682). These findings
validate our groups by indicating that visual imagery strength was objectively diminished in
aphantasics.
Autobiographical Memory Interview
We found stark differences between the AM reports of the aphantasics and controls. Figure 1A
and 1B display the comparison of the mean internal and external details between aphantasics
and controls for their descriptions of remote and recent memories on the AMI. On average, 2-
way ANOVA suggested that aphantasics described less internal details than controls, F(3, 81) =
22.4, p < .001, regardless of whether the memories were remote, p < .001, d = 1.25, or recent, p
= .001, d = 1.63. On the other hand, external details did not differ significantly between
aphantasics and controls, F(3, 81) = 0.16, p = .922, neither for remote, p = .938, d = 0.09, nor
recent memories, p = .992, d = 0.16.
We further compared different internal and external specific details acquired from
aphantasics and controls, as shown in Figure 1D. Specific internal detail categories showed
significant differences between aphantasics and controls (F(9, 641) = 117.1, p < .001), including
internal events, p < .001, d = 0.75, time, p = .435, d = 0.94, place, p = .058, d = 0.94,
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emotion/thought, p < .001, d = 1.15, and perception, p < .001, d = 1.17. However, for external
details, no significant differences were found between the two groups, F(7, 498) = 42.89, p <
.001, including external events, p = .970 d = 0.16, semantic details, p > .999, d = 0.01, repetition,
p = .997, d = 0.13, and other details, p = .998, d = 0.13.
Last, significant differences between aphantasics and controls were revealed for the
ratings of episodic richness, t(142.09) = 12.61, p < .001, d = 2.09, and for confidence, t(140.93) =
8.51, p < .001, d = 1.41 (see Figure 1C). When comparing self-reported visualization scores,
aphantasics rated their own memories as less visual, t(140.39) = 16.77, p < .001, d = 2.80.
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Figure 1. Behavioral AM deficits associated with aphantasia. (A) Mean amount (± SEM) of
internal details (B) and external details for recent and remote memories. (C) Episodic richness
and confidence scores for controls and aphantasics. (D) Specific internal and (E) external
memory detail categories for aphantasics and controls. * p < .05, ** p < .01, *** p < .001, ****
p < .0001, n.s. = non-significant.
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Behavioral results of the fMRI AM task
We found stark differences for the vividness response between groups, t(28) = 5.29, p < .001.
While controls reported in 86 % (SD = 26 %) of trials that their AM retrieval had been vivid,
aphantasics indicated only in 20 % (SD = 20 %) of trials that their AM retrieval had been vivid.
Moreover, aphantasics responded slower (M = 1.34 s, SD = 0.38 s) than controls (M = 1.00 s, SD
= 0.29 s) when they were asked if their retrieved memories were vivid or faint, t(28) = 2.78, p =
.009. In contrast, there were no differences between groups during the MA trials, neither on
the easy/hard response, t(28) = 1.16, p = .255, nor on the reaction times, t(28) = 0.58, p = .567.
Overall, participants engaged with a good response rate to the AM task in the scanner. There
were only 9 % missing values in AM trials and 7 % missing values in MA trials with no
differences of missing values between groups, neither for AM trials, t(19.98) = 1.11, p = .281,
nor for MA trials, t(18.13) = 0.52, p = .609.
Activation patterns associated with AM retrieval
Whole-brain activation during AM retrieval of both groups is displayed in Figure 2A and B.
Overall, both groups showed greater activation in all areas typically associated with AM,
including bilateral hippocampus, vmPFC, and medial/lateral parietal regions, during AM
retrieval in comparison to MA solving. When examining the difference in activation, aphantasics
displayed greater activation in the bilateral visual-perceptual regions (maximum in lingual
gyrus) in the occipital cortex than controls, t(28) = 4.41, p < .001 (MNI: right visual cortex: x =
12, y = -79, z = 5; left visual cortex: x = -9, y = -76, z = 29, see Figure 2C and D). In contrast,
controls showed greater activation in the right posterior hippocampus than aphantasics, t(28) =
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3.77, p < .001 (MNI: x = 39, y = -31, z = -13). An additional correlation analysis revealed that
those participants with higher visual-perceptual cortex activation had less hippocampal
activation, r(28) = -.39, p = .041.
Of note, in order to examine hippocampal activation in greater detail, we manually
segmented the hippocampus anatomically into left anterior, left posterior, right anterior and
right posterior parts (see Supplementary Material for Methods and Results). For each subject,
we then extracted fMRI signals during AM retrieval and MA. We found that aphantasics showed
less AM-associated activation in all hippocampal parts (see Supplementary Material: Figure S1).
Figure 2. Activation during AM retrieval. (A) Stronger activated cortical regions during AM
retrieval (in warm colors) in comparison to math problem solving (in cool colors) in aphantasics
(B) and controls. (C) Aphantasics showed greater activation in visual-perceptual cortices than
controls. (D) Controls showed stronger activation in the right posterior hippocampus than
aphantasics (D). Images thresholded at p < 0.001, cluster size 10, uncorrected, except (D) which
is thresholded at p < 0.01, clustersize 10, for display purposes.
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Exploring functional connectivity of hippocampus and visual-perceptual cortices during AM
and resting state
The whole-brain analyses strengthened our hypothesis that a core difference between
aphantasics and controls lies in the interplay between the visual-perceptual cortex and the
hippocampus. To test this interplay, we examined functional connectivity between the peak
differences of the hippocampus and visual-perceptual cortex during AM retrieval and resting
state (see Figure 3A and B). During AM retrieval, we found that aphantasics showed strikingly
stronger functional connectivity between the right hippocampus and bilateral visual-perceptual
cortices than controls (right visual cortex: t(28) = 2.31, p = .01; left visual cortex: t(28) = 2.65, p
= .006). However, this effect was not specific to AM retrieval, since aphantasics also showed
stronger resting-state connectivity between the right hippocampus and the left visual-
perceptual cortex than controls, t(29) = 2.83, p = .004.
In a next step, we examined whether functional connectivity between the right
hippocampus and visual-perceptual cortex carried information about one’s ability to visualize
AMs. While connectivity alone did not predict the visualization scores in the AMI, β = –.06, p =
.391, group allocation, β = .92, p < .001, and the interaction between group allocation and
connectivity, β = .26, p < .001, did (see Figure 3B). Interestingly, for controls, we found a
positive correlation between the resting-state connectivity of the right hippocampus and the
visual cortex and the visualization scores from the AMI, r(13) = .65, p = .011. On the other hand,
for aphantasics, we found a negative correlation between the resting-state connectivity of the
right hippocampi and the visual cortex and the visualization scores from the AMI, r(14) = -.57, p
= .027.
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Thus, our fMRI results indicate that aphantasics show an increased activation and
functional connectivity of the visual-perceptual cortex, and that this over-response seems to be
directly associated with the deficit in visualization of autobiographical events.
Figure 3. Functional connectivity between the visual-perceptual cortex and hippocampus
during AM retrieval and resting state. (A) During AM retrieval, stronger ROI-to-ROI
connectivity between the hippocampus and visual-perceptual cortex in aphantasics compared
to controls. (B) Resting-state functional connectivity between the visual-perceptual cortex and
hippocampus correlates with visualization abilities. Fitted straight lines indicate a negative
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correlation for aphantasics (red) and a positive correlation for controls (blue) between
visualization scores and functional connectivity.
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Discussion
In this study, we set out to examine the neural correlates of episodic AM retrieval in aphantasia
as a way to examine the influence of visual imagery on episodic AM. In line with previous
reports, we found that aphantasics reported less sensory details during AM retrieval regardless
of the recency of memory (cf. Dawes et al., 2020; 2022; Milton et al., 2020; Zeman et al., 2020).
Strikingly, the deficit in constructing visual imagery associated with aphantasia not only led to a
reduced retrieval of visual-perceptual details but to a broader impairment in retrieving episodic
AMs, including reduced emotions and confidence attached to the memories. Thus, in
agreement with a recent account of aphantasia (Blomkvist, 2022), our results support the idea
that a diminished construction of visual details during AM retrieval leads to a more general
episodic memory deficit. We expand the current knowledge by adding that this AM deficit is
reflected neurally by an increased activation and connectivity of the visual-perceptual cortex
and decreased activation of the hippocampus associated with aphantasia. Our findings provide
novel insights into three current debates: 1) the mechanisms of aphantasia-related AM deficits,
2) the similarities and differences between aphantasics and individuals with hippocampal
damage, and 3) the neural models of AM.
Potential mechanisms of aphantasia-related AM deficits
We report that aphantasics show increased activation of the visual-perceptual cortices as well
as decreased hippocampal activation during AM retrieval in comparison to controls. In addition,
aphantasics showed increased functional connectivity between the hippocampus and visual-
perceptual cortices during AM retrieval and resting-state, and the strength of this functional
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connectivity predicted worse visualization capacity. These findings fit well to previous
neuroimaging studies pointing towards a central role of the dynamic interplay between the
hippocampus and visual-perceptual cortex during AM retrieval (McCormick, et al. 2015). This
interplay seems to be especially important during the elaboration stage of AM retrieval, a
period when specific visual-perceptual details are being actively broad back into the mind’s eye.
At this point, it remains unclear whether the disruption of AM elaboration at the encoding,
storage or retrieval process.
Furthermore, increased fMRI activity in the visual-perceptual cortices in aphantasia has
been reported previously (Fulford et al., 2018; Keogh et al., 2020). A prominent hypothesis
states that this heightened activity of the visual-perceptual cortices hinders aphantasics to
detect small imagery-related signals (Pearson, 2019). Our findings support this hypothesis since
fMRI-dependent changes in visual-perceptual cortices were not exclusively seen during the AM
paradigm but were also present in the resting-state functional connectivity, indicating a more
generally heightened state of arousal rather than a memory-specific reaction. In our study,
increased visual-perceptual cortex connectivity during resting state directly correlated with
worse visualization scores in aphantasics. Thus, the increased activity and connectivity of the
visual-perceptual cortex may disrupt the much-needed dynamical exchange with the
hippocampus during the active attempt to retrieve visual-perceptual details for AMs.
The extended constructive episodic simulation hypothesis proposes a top-down hierarchy
during mental imagery (Blomkvist, 2020). In this model the hippocampus initiates retrieval
processes in primary sensory brain regions, such as the visual-perceptual cortex in order to
retrieve visual-perceptual details associated with a specific AM. Evidence for such top-down
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hierarchies during mental imagery have been observed in fronto-parietal and occipital networks
via effective connectivity analyses, such as Granger Causality and Dynamic Causal Modelling
(Dentico et al., 2014; Dijkstra et al., 2017; Mechelli et al., 2004). In aphantasia, it is
hypothesized that this top-down hierarchy is disrupted and therefore, the hippocampus can no
longer retrieve and incorporate visual-perceptual details in one coherent mental event.
Because of the slow temporal resolution of the fMRI sequence, our data cannot directly answer
the question of temporal directionality between the hippocampus and visual-perceptual cortex.
Nonetheless, our findings suggest that the bidirectional connectivity between both brain
structures is crucial for the re-experience of episodic AMs. As such, hippocampal memory
indices may be needed to retrieve specific details and if these details are not provided by the
visual-perceptual cortices, the entire episodic AM retrieval seems to fail.
Similarities and differences between aphantasics and individuals with hippocampal lesions
At face value, the selective episodic AM deficits reported previously (Dawes et al., 2020; 2022;
Milton et al., 2020; Zeman et al., 2020) and observed in our sample suggest that aphantasia is
an episodic memory condition, similar to the AM amnesia known from individuals with
hippocampal damage. In fact, aphantasics and individuals with hippocampal damage report less
internal details across memory detail subcategories (Rosenbaum et al., 2008; St-Laurent et al.,
2009; Steinvorth et al., 2005) and this deficit can be observed regardless of the recency of the
memory (Miller et al., 2020). These similarities suggest that aphantasics are not merely missing
the visual-perceptual details to specific AMs but they have a profound deficit associated with
the retrieval of AMs. However, there are also stark differences between aphantasics and
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individuals with hippocampal damage. Foremost, aphantasics seem not to have difficulties to
retrieve spatial information (Blomkvist, 2020), which is another inherent function of the
hippocampus (Burgess et al., 2002; O’Keefe, 1991), potentially relying on different paths
(Pearson, 2019). The scene construction theory states, that the hippocampus is crucially needed
for the construction of spatially coherent mental models of scenes (Maguire & Mullally, 2013).
For example, patients with hippocampal damage cannot imagine the spatial layout of fictitious
scenes (Hassabis et al., 2007), they detect less errors in spatially-incoherent scenes than
controls (McCormick et al., 2017), and they show less scene-dependent mind-wandering
episodes (McCormick, Rosenthal, et al., 2018). In the current study, we did not set out to
examine spatial cognition in aphantasics, however, parts of our data speak to this aspect. For
example, aphantasics did not differ from controls in their reported amount of spatial details on
the AMI. When asked in our debriefing questions, aphantasics explained that they know how
the space around them felt, they just cannot see it in front of their mind’s eye. In fact, one
aphantasic put her finger on it, describing it as: “I can put my consciousness in my kitchen at
home and feel all around but there is no visual image attached to this feeling.” Thus, we would
predict that aphantasics do not show any deficits in tasks that depend on hippocampal scene
construction processes. What could be impaired in aphantasics are all cognitive functions which
rely on the population of the constructed scenes with visual-perceptual details, such as episodic
AM retrieval, episodic future thinking, complex decision-making, and complex empathy tasks.
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Towards a novel neural model of autobiographical memory
While more research is required exploring the cognitive landscape associated with aphantasia,
such as spatial cognition and scene construction, our data contribute to an old debate of how
AM retrieval and visual imagery are intertwined. We propose that the hippocampus is
embedded in a brain-wide network, comprising the vmPFC and visual-perceptual cortices, in
which each of these nodes contributes specific processes to the re-construction of extended
detail-rich mental events (see also Ciaramelli et al., 2019; McCormick, Ciaramelli, et al., 2018).
Within this model, the vmPFC initiates and overseas the scene construction process which takes
place in the hippocampus. Judging from our data, these processes are not disturbed in
aphantasia. Further, the visual-perceptual cortex provides the visual details which are essential
to populate the hippocampal-constructed scenes. This model is backed up by a previous
dependent MEG study revealing that the vmPFC directs hippocampal activity during the
initiation of AM retrieval (McCormick et al., 2020). This finding has been replicated and
extended by Chen et al. (2021), showing that the vmPFC leads hippocampal involvement during
scene construction and other scene-based processes (Monk et al., 2021). On the other hand,
there are a few case reports of damage to the occipital cortex causing AM amnesia (Greenberg
et al., 2005), potentially by preventing the population of the hippocampally constructed scenes.
Indeed, our current study suggests that a reliable connectivity between the hippocampus and
the visual-perceptual cortices is essential to provide the visual details necessary for successful
vivid, detail-rich AM retrieval.
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Conclusion
Aphantasia provides a natural knock-out model for the influence of visual imagery on different
cognitive functions. We here report a tight link between visual imagery and our ability to
retrieve vivid and detail-rich personal past events, as aphantasics do not only report fewer
visual-perceptual details for episodic AMs but also show decreased confidence and
emotionality associated with the AMs. In this context, we highlight the central role of the
functional connectivity between the hippocampus and occipital cortex to assemble visual-
perceptual details into one coherent extended mental event. Exciting novel research avenues
will be to examine hippocampal-dependent spatial cognition in aphantasics and to investigate
whether neuroscientific interventions can be used to enhance AM retrieval by enhancing visual
imagery.
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Supplementary material
Native space hippocampal fMRI activation
Since our main goal was to assess hippocampal involvement during AM retrieval in aphantasia,
we sought to examine in depths whether there were any group differences in hippocampal
activation in respect to the hemispheric laterality or along its long-axis. For this analysis, we
used the anatomical hippocampal masks in native space and divided them into anterior and
posterior portions, using the location of the uncus as boundary, for both hemispheres. We then
extracted signal intensity values from these ROIs for each participant and each condition using
the MATLAB-based Response Exploration toolbox (REX; www.nitrc.org/projects/rex/). Potential
laterality effects and effects between the anterior and posterior hippocampus were assessed
using a 2-way ANOVA with a posthoc Tukey’s multiple comparison test, applying a significance
threshold of α = .05.
Differences in hippocampal activation during AM retrieval
We found stark group differences in hippocampal activation during AM versus MA. Aphantasics
showed reduced activation of bilateral hippocampi, F(17, 252) = 3.03, p < .001, including the left
anterior, left posterior, right anterior, and right posterior hippocampus (see Figure S1). There
was no laterality effect nor differences along the pattern of activation down the anterior-
posterior axis between the groups (all ps > .05). Together, these findings indicate that the
behavioral AM deficit associated with aphantasia is reflected neurally by a reduced bilateral
hippocampal activation.
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Figure S1. Reduced hippocampal activity during AM retrieval associated with aphantasia. The
signal intensities during AM and MA were extracted from the hippocampal masks created from
each individual participant. (A) An example of a 3D reconstruction of the hippocampus,
separated into anterior and posterior portions. (B) The comparison between the percentage of
signal change during the AM and MA tasks in the hippocampus of aphantasics and controls.
Aphantasics show reduced differentiation between AM and MA than controls in all portions of
the hippocampus. * p < .05.
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41
Table S1. Peak coordinates of the AM and MA activation for Aphantasia.
Region
Hemisphere
MNI Coordinates
Voxels
T-value
X
Y
Z
Activation AM > MA
Posterior Cingulate Gyrus
Right
18
-57
11
4657
11.00
Parahippocampual Gyrus*
Left
-21
-31
-13
9.06
Hippocampus
Left
-27
-17
-19
205
8.40
Superior Frontal Gyrus
Left
-12
47
50
926
8.38
Angular Gyrus
Left
-42
-55
23
165
7.88
Lateral Orbitofrontal Cortex
Left
-42
38
-16
208
7.58
Hippocampus
Right
18
-37
-1
199
6.89
Cerebellum
Right
15
-79
-37
109
6.33
Brainstem
Right
3
-46
-52
43
6.03
Parahippocampual Gyrus*
Right
24
-31
-13
6.02
Middle Temporal Gyrus
Right
60
2
--19
76
5.27
Supramarginal Gyrus
Right
54
-58
32
26
4.99
Middle Frontal Gyrus
Left
-39
20
50
12
4.52
Activation MA > AM
Precuneus
Left
-18
-58
41
594
-3.85
Inferior Temporal Gyrus
Right
51
-46
-13
123
-3.85
Precuneus
Right
24
-49
53
718
-3.85
Insula
Left
-30
23
11
48
-3.85
Inferior Temporal Gyrus
Left
-51
-49
-13
67
-3.86
Cerebellum
Right
30
-67
-52
27
-3.87
Middle Frontal Gyrus
Right
33
41
17
34
-3.87
Superior Frontal Gyrus
Right
30
5
59
52
-3.87
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Inferior Frontal Gyrus
Right
54
14
29
35
-3.88
Insula
Right
39
11
8
51
-3.88
Inferior Frontal Gyrus
Left
-57
11
26
182
-3.88
Lateral Globus Pallidus
Right
23
-7
14
14
-3.92
Cerebellum
Left
-24
-64
-46
16
-3.93
*Sub-cluster level, Cluster size = 10 voxels, p-value = 0.001
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43
Table S2. Peak coordinates of the AM and MA activation for healthy controls.
Region
Hemisphere
MNI Coordinates
Voxels
T-value
X
Y
Z
Activation AM > MA
Parahippocampal Gyrus
Right
27
-28
-19
11319
12.41
Parahippocampal Gyrus*
Left
-24
-25
-16
9.01
Cerebellum
Left
-18
-76
-37
108
7.67
Anterior Cingulate
Right
9
35
11
13
7.01
Medial Frontal Gyrus
Right
18
32
29
233
6.93
Inferior Frontal Gyrus
Right
60
32
11
53
5.94
Hippocampus
Left
-36
-22
-16
252
5.64
Hippocampus
Right
27
-22
-16
233
5.28
Hypothalamus
Right
3
-4
-10
16
4.93
Activation MA > AM
Post Central Gyrus
Left
-33
-43
62
643
-3.73
Precuneus
Right
21
-52
53
483
-3.74
Inferior Frontal Gyrus
Right
51
8
26
16
-3.74
Middle Occipital Gyrus
Right
33
-82
2
26
-3.75
Middle Temporal Gyrus
Left
-51
-58
-1
18
-3.76
*Sub-cluster level, Cluster size = 10 voxels, p-value = 0.001
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