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Procedia Computer Science 169 (2020) 787–794

Postproceedings of the 10th Annual International Conference on Biologically Inspired Cognitive

Architectures,
Postproceedings BICA
of the 10th 2019
Annual (Tenth Annual
International Meetingon
Conference of Biologically
the BICA Society)
Inspired Cognitive
Architectures, BICA 2019 (Tenth Annual Meeting of the BICA Society)
The architecture of neural networks for enhanced autobiographical
The architecture of neural
memory networks
access: for enhanced
a functional autobiographical
MRI study
memory access: a functionala,MRI study
Polina Zhigulina​, Vadim Ushakov​ , Sergey Kartashov​ , Denis Malakhov​, Vyacheslav
a​ a, c​ c​ a​

Orlov​
Polina , Konstantin
a​
Zhigulina​, Vadim
a​ Novikov​, Anna
d​ a, c​
Ushakov​ Korotkova​
, Sergey , Konstantin
a​
Kartashov​ , DenisAnokhin​
a, c​ , Veronika
b​ a​
Malakhov​ , Vyacheslav
a​ d​ Nourkova​ b a​
Orlov​, Konstantin Novikov​, Anna Korotkova​, Konstantin Anokhin​, Veronika b​

Nourkova​
NRC “Kurchatov
b
Institute”, Moscow Russia
a​

Lomonosov Moscow State University, Moscow, Russia

b ​

c​ NRC “Kurchatov
a​
National Research Nuclear University Institute”,
MEPhI (Moscow Moscow Russia
Engineering Physics Institute), Moscow, Russia
d​ Lomonosov
b ​
Skolkovo Moscow
Institute Stateand
of Science University, Moscow,
Technology, Russia
Moscow, Russia
c​
National Research Nuclear University MEPhI (Moscow Engineering Physics Institute), Moscow, Russia
d​
Skolkovo Institute of Science and Technology, Moscow, Russia

Abstract
Abstract
The paper reports results of the first neuroimaging study of a peculiar phenomenon of autobiographical human memory (AM) - a
state of “enhanced memory access”. The objective of this work was to determine the AM network and the AM gate, i.e. the brain
The paper responsible
structures reports results
forofaccess
the firsttoneuroimaging study ofnetwork.
the entire memory a peculiarInphenomenon of autobiographical
the framework human
of the experiment, fMRImemory
images (AM) -a
of the
state of “enhanced
volunteers' memory
brains were access”.
obtained The objective
during of this
normal and work was
enhanced to determine thememory
autobiographical AM network and the
retrieval, AMpre-processing
then gate, i.e. the brain
and
structures
processing responsible
of these dataforwere
access to the entire
performed, memory
the areas network.
involved In the framework
in actualization of the AMofonthe
theexperiment,
individual andfMRI images
group levelsofwere
the
volunteers' brains were obtained during normal and enhanced autobiographical memory retrieval, then pre-processing
identified, after that the connections between these areas were exposed and visualized, and a meta-analysis of the data received at and
processing level
individual of these
weredata were performed,
performed. The areasthethat
areas involved
were in actualization
identified in the state ofofenhanced
the AM on the individual
memory retrievaland group levels
significantly were
overlap
identified,
with after that
the already the connections
known AM network,between these areas
but activations werewere
alsoexposed
detectedand visualized,
in areas and a meta-analysis
not mentioned earlier in theofpapers
the data
onreceived
AM. Also at
individual level were performed. The areas that were identified in the state of enhanced memory
we report evidence, that achievement of the “enhanced memory access” has individual threshold for each subject.retrieval significantly overlap
with the already known AM network, but activations were also detected in areas not mentioned earlier in the papers on AM. Also
we report evidence, that achievement of the “enhanced memory access” has individual threshold for each subject.
© 2019 The Authors. Published by Elsevier B.V.
© 2020 The Authors. Published by Elsevier B.V.
This is
This is an open
open access
access article
article under
under the
the CC
CC BY-NC-ND
BY-NC-ND license
license (​https://creativecommons.org/licenses/by-nc-nd/4.0/​)
© 2019an The Authors.
Peer-review under Published
responsibilitybyofElsevier
the B.V. committee of(http://creativecommons.org/licenses/by-nc-nd/4.0/)
scientific the10th
9th Annual
Annual International
International Conference
Conference on
on Biologically
Biologically Inspired
Inspired
Peer-review
This under
is an open responsibility
access of the
article under the scientific
CC BY-NC-NDcommittee of the
license (​https://creativecommons.org/licenses/by-nc-nd/4.0/​)
Cognitive
Cognitive Architectures.
Architectures.
Peer-review under responsibility of the scientific committee of the 9th Annual International Conference on Biologically Inspired
Cognitive​memory;
Keywords: Architectures.
autobiography; fMRI; retrieval; neuroimaging; SPM; CONN

Keywords:​memory; autobiography; fMRI; retrieval; neuroimaging; SPM; CONN

1877-0509 © 2019 The Authors. Published by Elsevier B.V.

This is an open access article under the CC BY-NC-ND license (​ https://creativecommons.org/licenses/by-nc-nd/4.0/​
)
1877-0509
Peer-review©under
2019responsibility
The Authors. ofPublished by Elsevier
the scientific B.V.of the 9th Annual International Conference on Biologically Inspired Cognitive
committee
This is an open access article under the CC BY-NC-ND license (​
Architectures. https://creativecommons.org/licenses/by-nc-nd/4.0/​
)
Peer-review under responsibility of the scientific committee of the 9th Annual International Conference on Biologically Inspired Cognitive
Architectures.

1877-0509 © 2020 The Authors. Published by Elsevier B.V.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/)
Peer-review under responsibility of the scientific committee of the 10th Annual International Conference on Biologically Inspired
Cognitive Architectures.
10.1016/j.procs.2020.02.164
788 Polina Zhigulina et al. / Procedia Computer Science 169 (2020) 787–794
​4​ Zhigulina et al / Procedia Computer Science 00 (2019) 000–000

Fig. 1. Schematic of the brain regions typically involved in autobiographical memory retrieval. Ctx = cortex, PFC = prefrontal cortex. Original
publication in St. Jacques (2012).
1. Introduction

An important issue for a holistic model of human memory, which would integrate psychological, behavioral and
neurophysiological levels, is a problem of the relations between two modes of retrieval: serial and parallel retrieval.
Neurophysiological data provide evidence for the coexistence of serial and parallel processes within a cognitive
task as distinct processing stages. EEG and fMRI data show that at early stages of performing a dual-task brain
events corresponding with each of the task occur in parallel and then at response stage only the processing switches
to strictly serial strategy [1].
A fundamental problem behind this strategy is that working memory (WM) represent a bottleneck - everything
retrieved from long-term memory (LTM) has to go through WM to generate a conscious response. Since the
throughput of WM is limited to 3-5 units per time, the extreme processing power of brain highly constraints at the
level of awareness [2].
In accord with behavioral data on serial access to memory traces, much attention has been paid to studying
cortical regions, which are associated with retrieval of either discrete semantic knowledge [3][4][5] or single
experienced episodes, typically a list of previously exposed items [6].
Quite recently, there has been a detectable shift in the number of functional neuroimaging studies of
autobiographical memory, i.e. memory for significant events from one’s own personal past [7][8][9][10]. Despite
the challenge of controllability in eliciting ecological autobiographical memories in the scanning environment, the
autobiographical memory retrieval network was identified as a distributed set of primarily left-lateralized brain
regions (see Fig. 1.). This brain network encompasses cortical midline structures (ventral and dorsal Medial
Prefrontal Cortex, and Posterior Cingulate), ventral and dorsal Lateral Prefrontal Cortex, medial (i.e., Hippocampus)
and lateral Temporal Lobes, Temporoparietal Junction, and Cerebellum. It might be stressed, that autobiographical
memory has a dynamic localization, employing all regions mentioned above into the process of “on-line” memory
construction. The latter process seems to be highly dependent on activity at posterior Temporooccipital Networks
[11].
As it was noticed above all these data on the neural substrates of memory were obtained by scanning participants
while they recollected personal memories in response to cue words, accessing one memory per scan. In the present
study we examined whether it would be possible to evoke a parallel access to the content of more than one memory
at a time. Although due to WM limited capacity it seems impossible to be aware of more than one complex event
simultaneously, we speculated that providing a set of pre-trained verbal tags associated with the past personal events
could activate a brain state of “enhanced” memory access.
In this speculation we relied on so called “concentric” model of WM proposed by Oberauer [12] and Cowan [13].
In this model WM and LTM differ in the states of representations, not structurally. These differences may be
described as three regions: the focus of attention (FA), the direct-access region (DAR), the activated part of LTM
(aLTM), and the rest of LTM in passive state. It follows from the model that processing of activated items outside
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the region of WM direct access is approachable via associate links without complete awareness. Therefore, the state
of consciousness may be affected by a set of activated LTM items not present in the WM.
Hence, the main goal of the present study was to reveal neural networks underlying experience of parallel
awareness of more than one memory at a time during artificially evoked state of “enhanced” autobiographical
memory access.

Nomenclature

AM autobiographical memory
SDM self-defining memories
n(k) neutral stimulus of k two-words phrase
a(k) autobiographical stimulus of k phrases referred to SDM
ROI region of interest

2. Materials and Methods

The experiment involved 10 volunteers, each of whom gave an informed agreement to participate in the
experiment after being introduced to the experimental procedure. To evoke the target state of parallel access to
autobiographical memories we employed the original technique of simultaneous audio presentation of previously
trained verbal cues to self-defining memories (SDM). According to self-reports and eye-tracking data, this technique
proved to be effective in triggering a state being reported as simultaneous awareness of past episodes [14]. The
technique comprised four stages:
1. Each participant recollected eight SDMs, giving a privilege to memories addressing different life themes
and ages. The exact instruction was as follows: “Recollect, in as much detail as possible, eight episodes from your
past that represent to the maximum degree your personal traits and illustrate what kind of person you are”.
2. Each recollection was marked with unique cue two-word title.
3. The association of target recollection and cue title was tested three times successively. In each trial the
participants were asked to feel free to allocate as much time to complete visual image as they needed.
4. Each cue title was audio recorded separately while a participant loudly repeated it for 30 sec.
5. The audio records were superimposed on each other with a digital music editor AdobePremiereProCS3
Portable.exe. As a result all tags could be perceived by the listener simultaneously. It sounded like a “choir” of
verbal cues to personal memories.
6. For the control condition each participant read loudly a list of neutral phrases not associated with
autobiographical memories. Then they were elaborated as described above.
The scanning took place about a week after the collection of SDMs and training phase. At the main experiment
participants were presented with 5 conditions (n1-a1; n2-a2; n4-a4; n6-a6; n8-a8). In the n1-a1 condition the
participants were scanned while listening to the repetition of one isolated stimulus referred to SDM or listening to
two-word neutral phrase. In the n2-a2 condition the participants were scanned while listening to the repetition of two
superimposed “autobiographical” audio tracks or listening to two superimposed two-word neutral phrases. For the
rest of conditions the same logic was employed.
Experiment consisted of 4 series with randomization of stimulus order, 30 seconds were given for each stimulus
in the pair, between the series the rest time increased to 120 seconds. The experiment was performed on Magnetom
Verio 3T MR tomograph (Siemens, Germany) with the 32-channel head MR coil in NRC “Kurchatov Institute”. To
obtain high resolution anatomical MRI images, Т1-weighted sequence was used with the following parameters: TR
= 1900 ms, TE = 2.21 ms, 176 slices, voxel size: 1x1x1 mm3, slice thickness = 1 mm, flip angle = 9​ °,​inversion
time = 900 ms, and FOV = 320 mm​ . Functional MRI data was obtained on the basis of the EPI sequence with
2​
790 Polina Zhigulina et al. / Procedia Computer Science 169 (2020) 787–794
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following parameters: TR = 2000 ms, TE = 20 ms, 42 slices, voxel size: 2x2x2mm3, slice thickness = 2 mm, flip
angle = 90​°​, and FOV = 200 mm​ , ТА = 45 min 14 sec. For each subject 1350 functional images were obtained.
2​

Also, phase and magnitude images for Fieldmap correction were recorded with LongTE = 7.32 ms, ShortTE = 4.92
ms.
Data pre-processing and processing were performed using the SPM12 software package (statistical parametric
mapping: http://www.fil.ion.ucl.ac.uk/spm/).

2.1. Preprocessing of anatomical and functional images

Preprocessing consisted of the following steps. First, images reorientation was made in order to set the origin of
coordinates on the common point - anterior commissure. Secondly, we proceeded with artifacts cleaning: a phase
map was built based on phase and magnitude images for further correction of geometric distortions in functional
images caused by the inhomogeneity of the magnetic field; motion artifacts were eliminated by evaluating 6
parameters (3 displacements along the axes and 3 rotations around the axes), then comparing all images with the
first of the sequence and after that, applying the affine transformation, that "aligns" the images using interpolation
methods; also time heterogeneity correction was made for functional images. At the next step spatial normalization
was performed, i.e. mapping into standard anatomical space (MNI-space), made for both: anatomical and functional
images. At the end smoothing of functional slices using Gaussian function was made.

2.2. Data processing: individual and group analysis

Data processing for both individual and group analysis was performed using the General Linear Model.
Estimates of motion artifacts were added as additional regressors. Each column of the matrix corresponds to one
regressor, accordingly: conditions a1, n1, rest, 6 parameters of motion artifacts and a constant (average level of the
fMRI signal). In our experiment, 3 null hypotheses were tested: the absence of areas that 1) are activated during an
autobiographical auditory stimulus and are not activated during a neutral stimulus with the same number of words,
2) are activated during an autobiographical auditory stimulus and are not activated during rest, 3) are activated
during a neutral auditory stimulus and are not activated during rest. The contrast images were obtained based on
t-statistics with a threshold T = 4.3 (p-value = 0.001, without correction for multiple comparisons).
Contrast images obtained on the 1st level analysis were taken as data for the group level analysis. All subjects
were assigned to the same group for which total activation was observed. According to the results of a group level
analysis, for each contrast we defined common activation and disactivation of the brain regions for all subjects. The
threshold in this case was T = 4.3, which corresponds to p = 0.001 without correction for multiple comparisons.
Based on these data, we made masks, each disclosing one significant region (the biggest 4-5 for each contrast were
taken). The group analysis masks: a2-n2, a4-n4, a6-n6 and a8-n8 superimposed on the transparent brain common for
each contrast are shown in Fig. 1.

2.3. Correlations between brain regions

We applied CONN software (​ https://web.conn-toolbox.org/​), to search for correlations between brain regions.
Using CONN we performed 2 levels of analysis: individual and group on the different contrasts. The atlas used in
CONN maps 164 areas: 132 atlas (division into structures) and 32 network (allocation of areas included in the main
networks of the brain). We also added masks obtained on the previous step as regions of interest (ROIs). CONN
counts connection between the regions as a Fischer transformation z of the Pearson correlation coefficient r:

z = arctanh (r)

Such a transformation is normalizing and stabilizing dispersion. For more detailed information see Fisher [15].
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​a​ b​
Fig. 2. (a) group analysis mask, contrast a1-n1; (b) AM network, according to by Svoboda et al., 2006 [10]

3. Results

3.1. Group analysis

Based on group analysis we obtained masks for different contrasts. The contrast a1-n1 can be perceived as a
classic experiment of identifying active areas during an autobiographical retrieval using cue words. In this case, it
should be expected that obtained regions intersect with autobiographical memory network, obtained in previous
works. To verify this fact, we used a review article by Svoboda et al. [10], where autobiographical memory network
was extracted based on data from 24 AM studies. In Fig. 2. (b), taken from the work of Svoboda et al. [10], black
spots indicate the core of AM (areas mentioned in more than 10 studies), and others - secondary (5 or more studies)
and tertiary (- less than 5 studies) of the core, respectively. Fig. 2. (a) shows the mask obtained from a group
analysis of contrast a1-n1: the 5 largest clusters that are active during the actualization of the AM in the framework
of our experiment, are circled in Fig. 2. (a), and accordingly these areas are circled in Fig. 2. (b).
We can see activation in the right hemisphere of the Cerebellum, located closer to the center of the brain along the
x axis and slightly above the middle of the right hemisphere of the Cerebellum. Also, we can see activation in the
front of the left hemisphere closer to the center of the brain along the x axis, which is part of the Frontal Medial
Cortex and Frontal Orbital Cortex and Subcallosal Cortex. Then we notethe activation region located on the medial
surface of the left hemisphere - Temporal Gyrus. In the review [10], they were also referred to as AM core. The rest
of the circled areas indicate the regions in which activations were detected during our experiment but were not
highlighted in the review [10]. Both areas lie in the cortex of the right hemisphere: the higher one shows activation
of the Supramarginal Gyrus and Angular Gyrus, and the second one is structures of the Temporal Lobe - the
auditory areas: Planum Temporale, Heschl’s Gyrus, Temporal Gyrus. Also, slight activation can be observed in the
right lower Frontal Gyrus and in the Para-hippocampal Gyrus.
On the Fig. 3. masksare shown that were obtained from the group analysis of contrasts a2-n2, a4-n4, a6-n6 and
a8-n8. It can be noted that for contrasts a2-n2, a4-n4, a6-n6, the main activity falls on the auditory zones and the
areas responsible for performing audio-visual tasks: Planum Temporale - in the right and left hemispheres almost
equally, Heschl's Gyrus - in the left hemisphere is slightly larger, Central Opercular Cortex - mainly the right
792 Polina Zhigulina et al. / Procedia Computer Science 169 (2020) 787–794
​4​ Zhigulina et al / Procedia Computer Science 00 (2019) 000–000

hemisphere is F​ig. 3. Group analysis masks

.
involved, Superior Temporal Gyrus - lateralization is different for different contrasts, Planum Polare - in the right
hemisphere and in the left for contrast a2-n2, as well as Parietal Operculum Cortex for contrast a6-n6 in the left
hemisphere, and for contrast, a2-n2 in both. For contrast a8-n8 areas turned out to be completely different. The most
significant activation is observed in Precuneous Cortex - an area that is directly associated with episodic memory
and self-awareness processes. Large activations are also observed in the following areas: Lateral Occipital Cortex of
the left hemisphere, bilateral activation of Superior Parietal Lobule, Middle Temporal Gyrus, temporooccipital part
Left , Postcentral Gyrus Right and Central Opercular Cortex Right. The names of the areas were obtained using
ICNAtlas package (​ https://icnatlas.com/​
). Generally no visible activation during all contrasts except auditory zones
were found. Thus, further data analysis, i.e. searching for correlation, were proposed.

3.2. Correlations for each contrast - group level

This analysis was carried out under the assumption that the state of “enhanced memory access” was achieved by
each subject on each number of words. In this case, for each contrast we searched for correlations on the group level
using regions from the masks, obtained on previous step, as additional ROIs. The level of significance for
correlations was set by p = 0.001, 0.005 and 0.05 without FDR-correction. The idea was to extract a common
network among different contrasts.
For the thresholds of 0.001 and 0.005, there were too few correlating regions (no more than 1 for 0.001 and no
more than 6 for 0.005) and no intersections were found among them. On the other hand, for the threshold value of
0.05 quite a lot of areas were obtained, but without FDR-correction they cannot be considered as statistically
significant.

4. Discussion

For the classical experiment a1-n1, we obtained a significant overlap of the active regions with the AM core
identified in the meta-analysis by Svoboda et al. [10]: Cerebellum, Frontal Medial Cortex Frontal Orbital Cortex and
Subcallosal Cortex, left Temporal Gyrus. However, we also found brain regions that were not attributed to the AM
core: Supramarginal Gyrus, Angular Gyrus, and structures of the Temporal Lobe - Planum Temporale, Heschl’s
Gyrus Temporal Gyrus, all in the right hemisphere. In later studies by Bonnici et al.[16] and Silani et al. [17], the
role of Angular Gyrus and Supramarginal Gyrus in autobiographical retrieval processes was additionally
highlighted: it was suggested that these areas are responsible for the angle of the event reconstruction. There are
first-person and observer perspectives, depending on how one is reexperiencing the event. Activation of the Angular
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Gyrus is correlated with the subjective experience of past events, i.e. for a first-person perspective, and
Supramarginal Gyrus allows you to control the bias in social judgments and empathy. Activation in Planum
Temporale is observed not in the left hemisphere, where it is responsible for semantics, but in the right hemisphere,
where it is concerned with auditory attention [18]. Temporal Gyrus and Heschl’s Gyrus are also associated with
auditory processing and understanding of words’ meanings. Superior Temporal Gyrus activity is linked to emotional
perception, that is consistent for autobiographical retrieval.
According to the result of correlation search on the group level, we have to abandon the assumption that the state
of “enhanced memory access” was achieved among all subjects and at all contrasts. A more consistent hypothesis is
that the achievement of this state is specific for each person. Accordingly, a set of contrasts, in which it has been
achieved, varies from subject to subject. Under this assumption we are planning to perform further data-analysis.

Acknowledgements

This work was in part supported by the Russian Science Foundation, grant №18-11-00336 (data preprocessing
algorithms), by the Russian Foundation for Basic Research grant 17-29-02518ofi_m (cognitive brain architecture)
and by the Russian Foundation for Basic Research grant 18-00-00939 COMFI (algorithms for calculating).

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