Depression Identification Using EEG Signals Via A Hybrid of LSTM and Spiking Neural Networks
Depression Identification Using EEG Signals Via A Hybrid of LSTM and Spiking Neural Networks
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4726 IEEE TRANSACTIONS ON NEURAL SYSTEMS AND REHABILITATION ENGINEERING, VOL. 31, 2023
wavelet energy (RWE) and sample entropy were extracted SNNs, as computational models, encompass spiking neurons
and given to a two-layer feedforward ANN, achieving a as processing components, interconnected by biologically
classification accuracy rate of 98.11%. Acharya et al. [21] feasible learning algorithms [32], [33], [34]. SNNs inspired by
extracted a number of nonlinear features, such as detrended the brain have found utility across diverse domains, including
fluctuation analysis (DFA), fractal dimension, higher order but not limited to forecasting [35], simulation of the impact
spectra (HOS), Hurst’s exponent (HE), largest Lyapunov of mindfulness on individuals with depression [36], real-
exponent (LLE), recurrence quantification analysis (RQA), and world data classification, image recognition, odor recognition,
SampEn and fed them into five different classifiers. Using motor control, trajectory tracking, and more. In 2014,
a support vector machine (SVM) classifier, they reported Kasabov et al. introduced an SNN architecture called Neucube
an average accuracy of 98%. Raw EEG signals have been [37], designed to facilitate effective learning, modeling,
widely employed for classification using Artificial Neural and classification of spatiotemporal brain data (STBD).
Networks. For example, Acharya et al. [22] applied raw EEG Shah et al. [38] employed the SNN Neucube architecture to
signals to a 13-layer convolutional neural network (CNN) model and visualize brain activity in individuals displaying
and obtained classification accuracies of 93.5% and 96% over symptoms of depression. They utilized the dynamic evolving
the left and right hemispheres, respectively. Xia et al. [23] spiking neural network method (deSNN) for classification,
proposed an end-to-end integrated deep-learning model for achieving an accuracy of 68.18% for eyes-open state and
classifying major depressive disorder (MDD) patients and 72.13% for eyes-closed state. Despite the utilization of
healthy controls using raw EEG data. They achieved 91.06% brain-inspired SNNs for diverse spatiotemporal brain data
average accuracy. In another approach, Hashempour et al. [24] (STBD) modeling applications, a proficient supervised model
introduced a hybrid convolutional and temporal-convolutional for classifying Neucube’s output results has yet to be
neural network (CNN-TCN) to estimate the BDI score from introduced.
raw EEG signals in a continuous manner. Their method Despite growing interest in processing of EEG patterns for
achieved a mean squared error (MSE) of 5.64±1.6 and mean assessing depression, not many studies have scored the degree
absolute error (MAE) of 1.73±0.27 for the eyes-open state, of depression using EEG and more importantly, identifying
as well as an MSE of 9.53±2.94 and MAE of 2.32±0.35 for the brain mechanisms associated with different degrees
the eyes-closed state. of depression. However, such a research motivates further
Moreover, in [25], researchers introduced “DeprNet,” a deep development of this field by addressing these critical aspects.
learning-based CNN, achieving an accuracy of 0.91% and an To achieve this goal, we have utilized an extensive dataset
AUC of 0.95 in the classification of EEG data from both comprising EEG signals from 119 participants who underwent
depressed and normal subjects. Notably, their analysis of the the Beck test and were stratified into four depression levels:
final CNN layer visualization revealed that right electrodes minimum, mild, moderate, and severe. To estimate the
had higher prominence in depressed subjects, while left depression level, we present a novel methodology, combining a
electrodes exhibited greater prominence in normal subjects. brain-inspired SNN architecture with an LSTM neural network
In [26], an innovative automatic feature extraction method to model, visualize, learn, compare, and classify the subjects’
was employed using the Node2vec framework. This approach EEG signals. To compare the results of our method, we have
offered three fusion strategies: graph-level, feature-level, and also applied the raw EEG to a CNN-TCN, a CNN-LSTM, and
decision-level fusion, with a peak accuracy of 93.3% attained a 13-layer CNN network.
in the decision-level fusion process. In another study [27], The organization of this paper is outlined as follows:
a novel technique for extracting features from EEG signal Section II provides an overview of the dataset employed
channels has been developed. These features were integrated in this study, followed by a concise introduction to SNNs.
using a fuzzy ensemble strategy. In their method, they used Subsequently, we introduce a hybrid network that merges an
K-Nearest Neighbor classifier, which delivered the highest SNN architecture with an LSTM model. Section III presents
classification accuracy among the three datasets, with accuracy the visualization of the simulated network, accompanied by
scores of 91%, 96%, and 94%. Furthermore, [28] introduced a an analysis of the underlying brain structures associated with
dataset and employed traditional supervised machine learning depression. We present the empirical results, compare them to
algorithms to differentiate between healthy subjects and those state-of-the-art methods, and evaluate their respective strengths
with depression. Notably, the XGBoost classifier demonstrated and limitations. Finally, in Section IV, we conclude our study
the best performance, achieving an 87% accuracy rate for and outline avenues for future research.
the eyes-open (EO) state. These studies collectively exemplify
inventive methodologies and robust classification accuracy in
II. M ATERIALS AND M ETHODS
the domain of depression detection.
Although the mentioned methodologies have achieved A. Dataset Description and Preparation
commendable classification accuracy, none of them offered 1) Participants: We utilized an openly available dataset
model interpretations that could facilitate the identification from the PRED+CT website [39], initially comprising EEG
and comprehension of the brain mechanisms linked to recordings from 121 participants, including 72 females and
depression. While deep learning techniques draw inspiration 49 males. Subsequently, two subjects with incomplete practical
from certain observed properties in brain research [29], [30], information were identified and excluded from the analysis.
the latest generation of ANNs, called spiking neural networks All participants granted written informed consent, a protocol
(SNN) exhibits a greater degree of biological realism [31]. duly sanctioned by the University of Arizona’s ethics
SAM et al.: DEPRESSION IDENTIFICATION USING EEG SIGNALS VIA A HYBRID OF LSTM AND SNNs 4727
review process. The recruitment process involved enrolling mixtures and ICA for decomposition. It is important to note
individuals from introductory psychology courses, with the that HEOG and VEOG channels are initially dropped from the
selection based on their scores in the BDI mass survey. The analysis as they are not used for artifact removal. The artifacts,
eligibility criteria encompassed factors such as (a) age range which mainly include eye artifacts (such as blinks and eye
of 18 to 25 years, (b) absence of any history of head trauma movements), muscle artifacts, heart artifacts (ECG), and other
or seizures, and (c) no ongoing utilization of psychoactive non-neural artifacts, are eliminated using FastICA. The final
medications [40]. The recruited subjects exhibited diverse step involves back-projecting the remaining ICA components
levels of depression. Among the enrolled participants, 76 had into the channel space.
a Beck score ranging from 0 to 13, classifying them In the featured dataset, the training samples are not equally
into the control group (minimum depression). Furthermore, distributed across the target classes. Therefore, we employ
14 participants received scores ranging from 14 to 19 an undersampling technique in order to prevent the model
(indicating mild depression), 24 subjects attained scores from being biased toward the class that has a larger number
between 20 and 28 (reflecting moderate depression), and of training cases, which would reduce the model’s predictive
5 individuals scored within the range of 29 to 63 (indicative ability. To achieve this, an initial selection involves opting
of severe depression) [41]. for two minutes (equivalent to 30000 samples) of the EEG
2) Data Acquisition and Preprocessing: The dataset com- signal from both the eyes-open and eyes-closed states for
prised 500 seconds of recorded signals, acquired through each subject. Secondly, the signals are divided into five-
64 channels along with two additional channels, HEOG second windows (1250 samples), with each window having
and VEOG, following electrode settings aligned with the a 90% overlap. The 5-second window size has been chosen
10-20 standard EEG recording system [42]. The signals to accommodate SNNs that learn from spike occurrences.
were recorded during a resting state, utilizing a sampling In the absence of specific cognitive tasks during data
frequency of 500 Hz. The last two channels along with acquisition, this extended window supports more effective
the ‘CB1’ and ‘CB2’ channels are dropped, and ‘M1’ and unsupervised learning through spike-time dependent plasticity
‘M2’ are set as reference channels. This results in having (STDP) within the SNN reservoir. It allows for the capturing
a total number of 62 proper scalp channels. The recording of subtle temporal patterns and enhances the modeling of
paradigm encompassed events of both eyes-open and eyes- spatiotemporal EEG patterns, aligning with the network’s
closed conditions, exhibiting varying durations for different spike-driven processing. The data is then balanced across all
individuals. Consequently, the EEG data has been segregated depression levels based on the number of individuals. As a
into two distinct datasets: eyes-open and eyes-closed resting result, within each window, the data point count for depression
states. classes is normalized to align with the count of the class
In the initial stage, the EEG signal of each individual is possessing the smallest data point size. A data matrix with
partitioned into distinct event points. There are a total of the dimensions (4554, 1250, 62) and float type values is the
12 unique events within the signal. Due to variations in the result of this windowing operation.
number of occurrences for each event across different subjects,
differing quantities of segments are generated for each unique
event. In pursuit of dataset balance, we homogenize the B. Spiking Neural Networks
segment count for each distinct event to align with the In accordance with the all-or-none principle, information
minimum segment count of 120. The raw EEG signals within human brains is encoded through distinct events
are first preprocessed before being fed to the model. referred to as action potentials or spikes. A neuron generates a
To accomplish this, our methodology involves several steps. spike when its cumulative potential surpasses a predetermined
In the preliminary phase, we apply a downsampling of EEG threshold; otherwise, it continues to be inactive. Information
signals by a factor of two to reduce the data volume without regarding external stimuli and other internal computations
significantly violating the Nyquist rate. Subsequently, the is carried by the timing of spiking, the neuron’s location,
signal baselines are eliminated. Following this, a 50 Hz notch the neurons’ firing rate, and the temporal patterns. Due to
filter is employed, as outlined in [43] and [44], to counteract its binary information processing capability, SNN maintains
the power line interference. The signals then undergo bandpass its advantage in terms of energy efficiency and effectiveness
filtering, with cutoff frequencies set at 0.2 Hz and 50 Hz. over conventional ANNs [46], [47]. Incorporating a more
Lastly, the signals are processed using a Butterworth filter biologically realistic neuron model compared to traditional
with a fifth-order configuration, incorporating a high-cut ANNs [48], SNNs, as the third generation of neural network
at 50 Hz and a low-cut at 1 Hz. The filtered EEGs models, uniquely mimic the intricate mechanisms of the
are passed through independent component analysis (ICA) brain’s neurons. This inherent similarity to the brain’s neuron
in the last stage to remove any remaining undesirable mechanisms makes SNNs particularly well-suited for the
components. This study utilizes the MNE-python software analysis and modeling of EEG data. Operating across a
[45] to mitigate data contamination, primarily through a semi- multitude of spiking neurons, this model effectively processes
automated independent component analysis (ICA) approach. dynamic input information. The leaky-integrate and fire
In this context, we employ FastICA due to its notable model (LIF), a representation of a spiking neuron, can be
speed advantages over traditional ICA methods and its employed to emulate each neuron within the SNN model [49].
capability to accommodate non-Gaussianity. The procedure Notably, temporal dynamics are integrated into the operations,
involves principal component analysis (PCA) for whitening the alongside the synaptic states of the neurons. This temporal
4728 IEEE TRANSACTIONS ON NEURAL SYSTEMS AND REHABILITATION ENGINEERING, VOL. 31, 2023
various cognitive and computational tasks. where k ranges from 1 to the number of channels Nchannels =
The depression identification method proposed in this study 62, T is the signal length, and N represents the number of
is built upon a customized and improved version of the samples. X is a (T × Nchannels × N ) data matrix and VT
NeuCube framework [37]. This adaptation has been finely represents the resulting variable threshold array. Upon the
SAM et al.: DEPRESSION IDENTIFICATION USING EEG SIGNALS VIA A HYBRID OF LSTM AND SNNs 4729
Fig. 2. The architecture of the proposed method comprises three primary stages: EEG data encoding into spike trains, mapping to a 3-dimensional
brain-inspired SNN reservoir with 1471 neurons, and a two-step learning process for EEG dataset–unsupervised and supervised, ultimately leading
to classification.
occurrence of a rate of signal change surpassing the specific Algorithm 1 AER Spike Encoding
variable threshold in the kth input channel, a positive spike Require: X input ∈ RT ×Nchannels
is emitted. Conversely, when the rate of change breaches the Ensure: X Spike ∈ {0, 1}T ×Nchannels
variable threshold in a descending, or negative, direction, this 1: N ← #(X input ) ▷ Number of data samples in the dataset
triggers the generation of negative spikes. Algorithm 1 offers 2: for k = 1 to Nchannels do
a detailed exposition of this process, meticulously outlining 3: V T (k) ← 0
each step. 4: for i = 1 to N do
5: x ← channel k of the ith sample in X input
2) The 3D SNNr and Input Mapping: The 3D SNN 6: 1x T ×1 ← |δx|
reservoir (SNNr) module essentially constitutes an assemblage 7: µ ← mean(1x T ×1 )
of spiking neurons positioned spatially, with well-defined 8: σ ← st.dev.(1x T ×1 )
coordinates for the input neurons. This structure is designed 9: V Tk ← V Tk + (µ + σ )
to mimic the configuration of neurons within the brain. Here, 10: end for
we have implemented an SNNr with Nr eser voir = 1471 leaky 11: V Tk ← V Tk /N
12: end for
integrate and fire (LIF) model. These neurons are situated
13: for k = 1 to Nchannels do
in accordance with the Talairach Atlas [61], [62], forming 14: for i = 1 to N do
a cuboid shape resembling the human brain. Each neuron 15: x ← channel k of the ith sample in X input
represents 1 cm 3 brain area. The number of channels resulting 16: 1x T ×1 ← δx
from the loaded dataset, which in this case is Nchannels = 62, 17: xspike ← 0T ×1
defines the number of input neurons. The coordinates of these 18: for j = 2 to T do
input neurons are a subset of the SNNr coordinates. Using 19: if 1x j > V Tk then
the Koessler et al. mapping method [63], the nearest neuron 20: xspike ( j) ← 1
in the Talairach Atlas is allocated to the associated channel 21: end if
based on measurements of electrode placements, as shown in 22: end for
Fig. 3. Through the input neurons, the spike trains acquired 23: Store xspike in X Spike for channel k, sample i
following data encoding with the AER method are fed into 24: end for
25: end for
the SNNr.
An Nr eser voir × Nr eser voir matrix of distances called L dist
is created where an L2 norm is computed to determine
the distances between pairs of neurons. The “small world” connectivity (SWC) involves introducing a parameter for
connectedness tenet was selected based on the biological linking neurons within a defined range, referred to as the
process. Neighboring neurons become potentially coupled small-world radius (SWR). At the outset, all connections C(i j)
to one another as a result. The technique of small-world among the neurons within the entire reservoir are initialized to
4730 IEEE TRANSACTIONS ON NEURAL SYSTEMS AND REHABILITATION ENGINEERING, VOL. 31, 2023
Fig. 3. Utilizing the Talairach template coordinates, brain’s three-dimensional coordinates are assigned to the designated spiking neurons within
the SNNr. This procedure yields a three-dimensional SNNr structure that mimics the shape of the brain. Notably, red neurons (right) are designated
as input neurons and correspondingly map to the positions of 62 EEG channels (left).
1. If L dist (i j) > SW R, the connection status between the two Algorithm 2 SNNr Connection and Weight Initialization
neurons is marked as zero (disconnected). Each connection Require: X brain ∈ R1×3 , X input ⊂ X brain , C : 1 Nreservoir ×Nreservoir
between neurons i and j signifies i as the pre-synaptic neuron ▷ Hyperparameters: SW R
and j as the post-synaptic neuron. When a connection is Ensure: C : {0, 1} Nreservoir ×Nreservoir , W : R Nreservoir ×Nreservoir
deemed bidirectional, we randomly assign a value of 1 to one 1: Nr ← #(X brain ) ▷ Number of reservoir neurons
connection and a value of 0 to the other, thereby preserving 2: L dist is a matrix of distances between all pairs of neurons
only one of the two options. As a result, an SNNr with 3: for i = 1toNreservoir do
sparsely connected neurons is created. Our model’s SNN 4: for j = 1toNreservoir do
initialization is carried out by using the SWC connection 5: if L dist (i, j) > SW R then
rule with SW R = 2.5. After initialization, the weights of 6: Ci j ← 0
connections Wi j between the connected pairs of neurons (ij) 7: else
are established using the subsequent equation: 8: Wi j ← sgn(rand − 0.3) · rand · L dist1(i, j)
1 9: end if
Wi j = sgn (rand(1) − 0.3) . rand(1) . (7) 10: if Ci j = 1andC ji = 1 then
L dist (i j)
11: if rand < 0.5 then
where rand(1) generates pseudorandom values drawn from the 12: Ci j ← 0
standard uniform distribution within the open interval of 0 to 1. 13: Wi j ← 0
According to (7), the matrix W is expected to contain around 14: else
70% positive and 30% negative weights. In Algorithm 2, 15: C ji ← 0
we present an in-depth account of this procedure, leaving no 16: W ji ← 0
room for ambiguity. 17: end if
3) Unsupervised Learning in SNNr and Visualization: This 18: end if
methodology divides the learning process into two phases: 19: end for
unsupervised learning and supervised learning. The process 20: end for
of unsupervised learning is employed to adapt the initial
connection weights of the SNNr model as the model learns
from the continuous EEG data presented in the form of presynaptic neuron fires and neuron j is not in the refractory
spikes. The STDP rule, an unsupervised learning technique time:
with biological plausibility, is employed for this learning
process. The STDP mechanism regulates the synaptic strength P j (t) = P j (t − 1) + Wi j (8)
based on the temporal relationship between presynaptic and
During any given moment t, if a neuron’s potential surpasses
postsynaptic action potentials. This algorithm operates with
the firing threshold potential β, the neuron fires, leading to its
the utilization of the subsequent parameters:
potential Pk (t) being reset to 0. Concurrently, its refractory
• N iter : number of training iterations
counter Rk is established at R (refractory time). Conversely,
• β: spike generation threshold
if neuron k fails to achieve the firing threshold potential at
• η: learning rate
time t, its potential is diminished by the leak rate D, and its
• R: the resting period between spikes
refractory counter is updated:
• D: the leakage rate of neurons’ potential while inactive
Nchannels spike states are sent to the associated input Pk (t) = Pk (t − 1) − D (9)
neurons within the SNNr at each time step and potential Rk = Rk − 1 (10)
propagations are computed. Take the (i, j) neuron pair as
an example, where i represents the pre-synaptic neuron and Based on the STDP model grounded in the Hebbian learning
j represents the post-synaptic neuron. In the event when a rule, an increase in the connection weight between two neurons
SAM et al.: DEPRESSION IDENTIFICATION USING EEG SIGNALS VIA A HYBRID OF LSTM AND SNNs 4731
TABLE III
D ETAILED PARAMETERS S ETTINGS OF THE LSTM M ODULE
Fig. 5. The connectivity results from four distinct SNNr modules in the eyes-closed state are depicted. For each SNNr, the top 500 strongest
connections are showcased. Positive (excitatory) connections are portrayed with blue lines, whereas negative (inhibitory) connections are
represented by red lines. The brightness of each neuron corresponds to its spike emission level: (a) minimal depression; (b) mild depression;
(c) moderate depression; (d) severe depression.
Fig. 6. The connectivity results from four distinct SNNr modules in the eyes-open state are depicted. For each SNNr, the top 500 strongest
connections are showcased. Positive (excitatory) connections are portrayed with blue lines, whereas negative (inhibitory) connections are
represented by red lines. The brightness of each neuron corresponds to its spike emission level: (a) minimal depression; (b) mild depression;
(c) moderate depression; (d) severe depression.
new connections to cope with the challenges posed by the and C3 and PO3 in both eyes-closed and eyes-open states.
condition. In contrast, for individuals with severe depression, strong
In Fig. 7 and 8 we present graphical representations of connections were identified between F5 and T7, FT8 and F6,
the brain’s 62 electrodes, based on the standard 10-20 EEG FT8 and T8, as well as T8 and PO8.
electrode system, for four levels of depression during both The results align with the findings regarding the differences
eyes-closed and eyes-open states. Notably, our results reveal a between eyes-closed and eyes-open states. In the eyes-open
remarkable increase in connections related to the frontal and state, there are more sparse connections, including long-range
prefrontal cortex regions as depression becomes more severe. connections. This alignment is consistent with the notion
This finding suggests that depression may have a specific that the brain integrates information from distant regions to
impact on the connectivity within these brain areas, which process sensory inputs. Thus, during eyes-open states, the
are known for their involvement in cognitive and emotional brain’s functional connectivity involves a broader network of
processing. Moreover, as the depression level increases, the brain regions communicating over longer distances to handle
connections tend to become less sparse but rather stronger. external sensory information. Conversely, during eyes-open
This indicates that more connections are formed, and existing states, the sparsity observed is in line with the understanding
connections become more robust, potentially reflecting a that synchronization and coherence may be weaker due
reorganization of neural communication during depressive to the brain’s active engagement in processing sensory
states. In the minimally depressed group, robust connections information. The weaker synchronization and coherence
were consistently observed between F6 and PO3, F6 and FT8, during these periods could lead to more isolated and less
4734 IEEE TRANSACTIONS ON NEURAL SYSTEMS AND REHABILITATION ENGINEERING, VOL. 31, 2023
Fig. 7. The graphs effectively encapsulated the overall spike interaction during the eyes-closed state across regions within the SNN models,
symbolizing the 62 EEG channels as input neurons, throughout the STDP learning process for: (a) minimal depression; (b) mild depression;
(c) moderate depression; (d) severe depression. The nodes within the graphs depict the areas of input neurons in the SNN model, while the
thickness of lines represents the degree of spike transmission between these neuron areas (clusters). These clusters correspond to the input
neurons (EEG channels).
Fig. 8. The graphs effectively encapsulated the overall spike interaction during the eyes-open state across regions within the SNN models,
symbolizing the 62 EEG channels as input neurons, throughout the STDP learning process for: (a) minimal depression; (b) mild depression;
(c) moderate depression; (d) severe depression. The nodes within the graphs depict the areas of input neurons in the SNN model, while the
thickness of lines represents the degree of spike transmission between these neuron areas (clusters). These clusters correspond to the input
neurons (EEG channels).
Fig. 9. Correlation between each channel’s weighted degree centrality and depression severity for eyes-closed state.
coordinated neural activities, resulting in a sparser connectivity frontal and prefrontal cortex regions. Channels with low
pattern. correlation in the non-depressed group might play a crucial
In Fig. 9 and 10, we show the correlation between each role in maintaining emotional balance, while their weakening
channel’s weighted degree centrality and depression severity. connectivity may contribute to depressive symptoms. Channels
Channels FP1, Fpz, F3, PO5, and CP2 demonstrated the with higher correlation may be more directly related to
lowest correlation, suggesting that their connectivity weakens depressive symptoms, indicating their potential relevance in
as depression worsens. Conversely, channels AF3, AF4, F5, depression manifestation and progression.
F1, FT8, POz, and CP4 exhibited the highest correlation,
indicating a stronger association with depression severity. B. Classification Results
These findings suggest that depression level significantly To assess the classification efficacy of our proposed model,
impacts brain network connectivity, particularly involving the we conduct a comparative analysis with three well-established
SAM et al.: DEPRESSION IDENTIFICATION USING EEG SIGNALS VIA A HYBRID OF LSTM AND SNNs 4735
Fig. 10. Correlation between each channel’s weighted degree centrality and depression severity for eyes-open state.
Fig. 11. The averaged confusion matrixes for eyes-closed state along with the averaged accuracies for different models: (a) Proposed Model;
(b) Hashempoor et al., 2021; (c) Ay et al., 2019; (d) Achariya et al., 2018.
Fig. 12. The averaged confusion matrixes for eyes-open state along with the averaged accuracies for different models: (a) Proposed Model;
(b) Hashempoor et al., 2021; (c) Ay et al., 2019; (d) Achariya et al., 2018.
deep learning-based models using the same dataset. The first can be attributed to the model’s effective feature extraction,
model under consideration is the hybrid deep CNN-TCN specifically related to potential connectivity relationships
network, introduced by Hashempour et al. [24]. The second among different EEG channels, achieved through STDP
model combines a convolutional neural network with long unsupervised learning. The model’s biological plausibility
short-term memory (CNN-LSTM), as proposed by Ay et al. is a key advantage, as it is well-suited for processing
[69]. Lastly, we examine a 13-layer deep CNN presented biological EEG signals. This biologically-inspired approach
by Achariya et al. [22]. By juxtaposing our proposed model likely contributes significantly to the improved performance
against these prominent benchmarks, we aim to gain insights compared to alternative methods, aligning well with the
into its performance and potential advantages over existing inherent characteristics of EEG data. The utilization of
state-of-the-art approaches. just one LSTM layer to classify the output of SNNr
The model evaluation utilizes a 10-fold cross-validation further substantiates the efficacy of this biologically-inspired
procedure, with 10% of the subjects used as the testing approach.
set in each iteration. It is important to note that the
unsupervised learning step is conducted using the entire IV. C ONCLUSION
dataset in a single step, considering the time-consuming nature This study investigates the potential of depression recogni-
of this process. The aggregate performance is calculated by tion through the utilization of a novel combination of LSTM
averaging the outcomes from all ten evaluations. The results and SNN. For the first time, these models are employed
are showcased and compared in Fig. 11 and Fig. 12. The to model, map, learn, classify, visualize, and comprehend
results clearly indicate that our proposed model surpasses the EEG signals associated with four distinct depression levels,
other three models in classification accuracy. This success namely minimum, mild, moderate, and severe. The proposed
4736 IEEE TRANSACTIONS ON NEURAL SYSTEMS AND REHABILITATION ENGINEERING, VOL. 31, 2023
model integrates diverse methods and algorithms that facilitate [11] K. Sadatnezhad, R. Boostani, and A. Ghanizadeh, “Proposing an
the exploration and investigation of multiple aspects within adaptive mutation to improve XCSF performance to classify ADHD
and BMD patients,” J. Neural Eng., vol. 7, no. 6, Dec. 2010,
EEG data. This encompasses the spatial mapping of data Art. no. 066006.
onto a three-dimensional SNN structure, unsupervised learning [12] F. C. Morabito et al., “Deep learning representation from elec-
within the SNNr, visualization of connectivity and spiking troencephalography of early-stage Creutzfeldt–Jakob disease and
features for differentiation from rapidly progressive dementia,” Int.
patterns within the trained SNNr to unveil novel insights J. Neural Syst., vol. 27, no. 2, Mar. 2017, Art. no. 1650039, doi:
into the data and underlying brain mechanisms, along with 10.1142/s0129065716500398.
supervised learning within an LSTM network. Comparative [13] S. Kouchaki, R. Boostani, and F. Razavipour, “Fatigue detection using
analysis with other deep learning techniques showcases the the strength of dominant EEG source: A beamforming approach,”
Biomed. Eng., Appl., Basis Commun., vol. 30, no. 3, Jun. 2018,
advantages of employing the SNN approach in modeling time- Art. no. 1850023.
space brain data. This study not only achieves improved [14] F. Razavipour, R. Boostani, S. Kouchaki, and S. Afrasiabi, “Comparative
accuracy in classifying samples from different subject groups application of non-negative decomposition methods in classifying
fatigue and non-fatigue states,” Arabian J. Sci. Eng., vol. 39, no. 10,
but also reveals informative patterns of brain activities, pp. 7049–7058, Oct. 2014.
shedding light on the understanding of different severity of [15] F. Karimzadeh, M. Nami, and R. Boostani, “Sleep microstructure
depression. Our findings unveil significant differences between dynamics and neurocognitive performance in obstructive sleep apnea
different depression levels that hold promise as potential syndrome patients,” J. Integrative Neurosci., vol. 16, no. 2, pp. 127–142,
Feb. 2018.
markers for early prediction and prevention of depression. The [16] R. Boostani, F. Karimzadeh, and M. Nami, “A comparative review on
proposed methodology exhibits wide applicability to diverse sleep stage classification methods in patients and healthy individuals,”
neuroimaging and clinical longitudinal data. Future work will Comput. Methods Programs Biomed., vol. 140, pp. 77–91, Mar. 2017.
focus on refining SNN hyper-parameter optimization, further [17] F. Alimardani and R. Boostani, “DB-FFR: A modified feature selection
algorithm to improve discrimination rate between bipolar mood disorder
enhancing the visualization and analysis of the brain-structured (BMD) and schizophrenic patients,” Iranian J. Sci. Technol., Trans.
SNN during both the learning process and post-learning phase Electr. Eng., vol. 42, no. 3, pp. 251–260, Sep. 2018.
to deepen our comprehension of brain processes related to [18] D. Jarchi, R. Boostani, M. Taheri, and S. Sanei, “Seizure source
localization using a hybrid second order blind identification and
depression. Furthermore, the exploration of larger and well- extended rival penalized competitive learning algorithm,” Biomed. Signal
balanced datasets, as well as task-specific EEG signals, will Process. Control, vol. 4, no. 2, pp. 108–117, Apr. 2009.
be undertaken to delve into the impact of varying tasks on the [19] M. Cukic, M. Stokic, S. Simic, and D. Pokrajac, “The successful
analysis. This approach seeks to comprehensively investigate discrimination of depression from EEG could be attributed to proper
feature extraction and not to a particular classification method,” Cognit.
the effects of different tasks on the model’s performance and Neurodynamics, vol. 14, no. 4, pp. 443–455, Aug. 2020.
insights. [20] S. D. Puthankattil and P. K. Joseph, “Classification of EEG signals
in normal and depression conditions by ANN using RWE and
signal entropy,” J. Mech. Med. Biol., vol. 12, no. 4, Sep. 2012,
R EFERENCES Art. no. 1240019.
[21] U. R. Acharya, V. K. Sudarshan, H. Adeli, J. Santhosh, J. E. W. Koh, and
[1] Depression and Other Common Mental Disorders: Global Health A. Adeli, “Computer-aided diagnosis of depression using EEG signals,”
Estimates, World Health Organization, Geneva, Switzerland, 2017. Eur. Neurol., vol. 73, nos. 5–6, pp. 329–336, 2015.
[Online]. Available: https://apps.who.int/iris/handle/10665/254610 [22] U. R. Acharya, S. L. Oh, Y. Hagiwara, J. H. Tan, H. Adeli, and
[2] Y. Takahashi, “Depression and suicide,” Jpn. Med. Assoc. J., vol. 44, D. P. Subha, “Automated EEG-based screening of depression using deep
no. 8, pp. 359–363, 2001. convolutional neural network,” Comput. Methods Programs Biomed.,
[3] A. T. Beck, R. A. Steer, and G. Brown, Manual For The Beck Depression vol. 161, pp. 103–113, Jul. 2018.
Inventory-II. San Antonio, TX, USA: Psychological Corporation, 1996, [23] M. Xia, Y. Zhang, Y. Wu, and X. Wang, “An end-to-end
doi: 10.1037/t00742-000. deep learning model for EEG-based major depressive disorder
[4] K. L. Smarr and A. L. Keefer, “Measures of depression and classification,” IEEE Access, vol. 11, pp. 41337–41347, 2023, doi:
depressive symptoms: Beck depression Inventory-II (BDI-II), center for 10.1109/ACCESS.2023.3270426.
epidemiologic studies depression scale (CES-D), geriatric depression [24] S. Hashempour, R. Boostani, M. Mohammadi, and S. Sanei, “Continuous
scale (GDS), hospital anxiety and depression scale (HADS), and patient scoring of depression from EEG signals via a hybrid of convolutional
health Questionnaire-9 (PHQ-9),” Arthritis Care Res., vol. 63, no. 11, neural networks,” IEEE Trans. Neural Syst. Rehabil. Eng., vol. 30,
pp. 454–466, Nov. 2011. pp. 176–183, 2022, doi: 10.1109/TNSRE.2022.3143162.
[5] R. P. N. Rao, Brain-Computer Interfacing: An Introduction. [25] A. Seal, R. Bajpai, J. Agnihotri, A. Yazidi, E. Herrera-Viedma, and
U.K.: Cambridge Univ. Press, 2011, ch. 3.1.12, p. 26, doi: O. Krejcar, “DeprNet: A deep convolution neural network framework for
10.1017/CBO9781139032803. detecting depression using EEG,” IEEE Trans. Instrum. Meas., vol. 70,
[6] M. Wang and J. Y. Chen, “A GMM-IG framework for selecting genes pp. 1–13, 2021, doi: 10.1109/TIM.2021.3053999.
as expression panel biomarkers,” Artif. Intell. Med., vol. 48, nos. 2–3, [26] S. Soni, A. Seal, A. Yazidi, and O. Krejcar, “Graphical representation
pp. 75–82, Feb. 2010, doi: 10.1016/j.artmed.2009.07.006. learning-based approach for automatic classification of electroencephalo-
[7] A. Kolahi, M. Hoviattalab, T. Rezaeian, M. Alizadeh, M. Bostan, and gram signals in depression,” Comput. Biol. Med., vol. 145, Jun. 2022,
H. Mokhtarzadeh, “Design of a marker-based human motion tracking Art. no. 105420, doi: 10.1016/j.compbiomed.2022.105420.
system,” Biomed. Signal Process. Control, vol. 2, no. 1, pp. 59–67, [27] S. Soni, A. Seal, S. K. Mohanty, and K. Sakurai, “Electroencephalog-
Jan. 2007, doi: 10.1016/j.bspc.2007.02.001. raphy signals-based sparse networks integration using a fuzzy ensemble
[8] M. Sabeti, R. Boostani, and T. Zoughi, “Using genetic programming to technique for depression detection,” Biomed. Signal Process. Control,
select the informative EEG-based features to distinguish schizophrenic vol. 85, Aug. 2023, Art. no. 104873, doi: 10.1016/j.bspc.2023.104873.
patients,” Neural Netw. World, vol. 22, no. 1, pp. 3–20, 2012. [28] A. Seal et al., “Benchmarks for machine learning in depression discrim-
[9] B. Kazimipour, R. Boostani, A. Borhani-Haghighi, S. Almatarneh, and ination using electroencephalography signals,” Int. J. Speech Technol.,
M. Aljaidi, “EEG-based discrimination between patients with MCI vol. 53, no. 10, pp. 12666–12683, May 2023, doi: 10.1007/s10489-022-
and Alzheimer,” in Proc. Int. Eng. Conf. Electr., Energy, Artif. Intell. 04159-y.
(EICEEAI), Nov. 2022, pp. 1–5. [29] A. L. Hodgkin, A. F. Huxley, and B. Katz, “Measurement of
[10] K. Sadatnezhad, R. Boostani, and A. Ghanizadeh, “Classification of current-voltage relations in the membrane of the giant axon of
BMD and ADHD patients using their EEG signals,” Exp. Syst. Appl., Loligo,” J. Physiol., vol. 116, no. 4, pp. 424–448, Apr. 1952, doi:
vol. 38, no. 3, pp. 1956–1963, Mar. 2011. 10.1113/jphysiol.1952.sp004716.
SAM et al.: DEPRESSION IDENTIFICATION USING EEG SIGNALS VIA A HYBRID OF LSTM AND SNNs 4737
[30] J. E. Hall, Guyton and Hall Textbook of Medical Physiology, 13th ed. [50] E. Tu et al., “NeuCube(ST) for spatio-temporal data predictive modelling
Amsterdam, The Netherlands: Elsevier, 2015. with a case study on ecological data,” in Proc. Int. Joint Conf. Neural
[31] W. Maass, “Networks of spiking neurons: The third generation of neural Netw. (IJCNN), Jul. 2014, pp. 638–645.
network models,” Neural Netw., vol. 10, no. 9, pp. 1659–1671, 1997, [51] M. G. Doborjeh, E. Capecci, and N. Kasabov, “Classification and
doi: 10.1016/S0893-6080(97)00011-7. segmentation of fMRI spatio-temporal brain data with a NeuCube
[32] T. Masquelier, R. Guyonneau, and S. J. Thorpe, “Competitive STDP- evolving spiking neural network model,” in Proc. IEEE Symp.
based spike pattern learning,” Neural Comput., vol. 21, no. 5, Evolving Auto. Learn. Syst. (EALS), Orlando, FL, USA, Dec. 2014,
pp. 1259–1276, May 2009, doi: 10.1162/neco.2008.06-08-804. pp. 73–80.
[33] S. Thorpe and J. Gautrais, “Rank order coding,” in Computational [52] N. Kasabov, “Brain-, gene-, and quantum inspired computational intelli-
Neuroscience. Berlin, Germany: Springer, 1998, pp. 113–118. gence: Challenges and opportunities,” in Challenges for Computational
[34] A. Tavanaei, M. Ghodrati, S. R. Kheradpisheh, T. Masquelier, and Intelligence, vol. 63, W. Duch and J. Mandziuk, Eds. Berlin, Germany:
A. Maida, “Deep learning in spiking neural networks,” Neural Netw., Springer, 2007, pp. 81–97, doi: 10.1007/978-3-540-71984-7_9.
vol. 111, pp. 47–63, Mar. 2019. [53] I. J. Goodfellow et al., “Challenges in representation learning: A report
[35] R. Mohanty, A. Priyadarshini, V. S. Desai, and G. Sirisha, “Appli- on three machine learning contests,” Neural Netw., vol. 64, pp. 59–63,
cations of spiking neural network to predict software reliability,” in Apr. 2015, doi: 10.1016/j.neunet.2014.09.005.
Intelligent Engineering Informatics, vol. 695. Singapore: Springer, 2018, [54] B. Petro, N. Kasabov, and R. M. Kiss, “Selection and optimization of
pp. 149–157. temporal spike encoding methods for spiking neural networks,” IEEE
[36] Z. Doborjeh et al., “Spiking neural network modelling approach reveals Trans. Neural Netw. Learn. Syst., vol. 31, no. 2, pp. 358–370, Feb. 2020,
how mindfulness training rewires the brain,” Sci. Rep., vol. 9, no. 1, doi: 10.1109/TNNLS.2019.2906158.
p. 6367, Apr. 2019. [55] S. M. Bohte, “The evidence for neural information processing with
[37] N. Kasabov et al., “Evolving spatio-temporal data machines based on the precise spike-times: A survey,” Natural Comput., vol. 3, no. 2,
NeuCube neuromorphic framework: Design methodology and selected pp. 195–206, 2004, doi: 10.1023/B:NACO.0000027755.02868.60.
applications,” Neural Netw., vol. 78, pp. 1–14, Jun. 2016. [56] M. Ghesmoune, M. Lebbah, and H. Azzag, “A new growing neural gas
[38] D. Shah, G. Y. Wang, M. Doborjeh, Z. Doborjeh, and N. Kasabov, for clustering data streams,” Neural Netw., vol. 78, pp. 36–50, Jun. 2016,
“Deep learning of EEG data in the NeuCube brain-inspired spiking doi: 10.1016/j.neunet.2016.02.003.
neural network architecture for a better understanding of depression,” in [57] N. Nuntalid, K. Dhoble, and N. Kasabov, “EEG classification with
Neural Information Processing (Lecture Notes in Computer Science), BSA spike encoding algorithm and evolving probabilistic spiking neural
vol. 11955. Berlin, Germany: Springer, Dec. 2019, pp. 62–76, doi: network,” in Proc. Int. Conf. Neural Inf. Process. (ICONIP). Berlin,
10.1007/978-3-030-36718-3_17. Germany: Springer, 2011, pp. 451–460.
[39] J. F. Cavanagh, A. Napolitano, C. Wu, and A. Mueen, “The [58] T. Delbruck. (2007). JAER Open Source Project. [Online]. Available:
patient repository for EEG data + computational tools (PRED+CT),” http://jaer.wiki.sourceforge.net
Frontiers Neuroinform., vol. 11, p. 67, Nov. 2017. [Online]. Available: [59] P. Lichtsteiner and T. Delbruck, “A 64×64 AER logarithmic temporal
http://predict.cs.unm.edu/downloads.php derivative silicon retina,” Res. Microelectron. Electron., vol. 2,
[40] J. F. Cavanagh, A. W. Bismark, M. J. Frank, and J. J. B. Allen, “Multiple pp. 202–205, Jul. 2005.
dissociations between comorbid depression and anxiety on reward and [60] C. Tan, M. Sarlija, and N. Kasabov, “Spiking neural networks:
punishment processing: Evidence from computationally informed EEG,” Background, recent development and the NeuCube architecture,” Neural
Comput. Psychiatry, vol. 3, pp. 1–17, Jan. 2019. Process. Lett., vol. 52, no. 2, pp. 1675–1701, Oct. 2020.
[41] M. Tohen, C. Bowden, A. A. Nierenberg, and J. Geddes, Clinical [61] J. L. Lancaster et al., “Automated Talairach atlas labels for functional
Trial Design Challenges in Mood Disorders. Cambridge, MA, USA: brain mapping,” Hum. Brain Mapping, vol. 10, no. 3, pp. 120–131, 2000.
Academic Press, 2015. [62] J. L. Lancaster et al., “Automated labeling of the human brain:
[42] G. H. Klem, H. O. Lüeders, H. H. Jasper, and C. Elger, “The ten-twenty A preliminary report on the development and evaluation of a
electrode system of the international federation,” Electroencephalogr. forward-transform method,” Hum. Brain Mapping, vol. 5, no. 4,
Clin. Neurophysiol., vol. 52, no. 3, pp. 3–6, 1999. pp. 238–242, 1997.
[43] A. Zajac and P. Paszkiel, “Using brain-computer interface technology [63] L. Koessler et al., “Automated cortical projection of EEG sensors:
as a controller in video games,” Informatyka, Automatyka, Pomiary w Anatomical correlation via the international 10–10 system,” NeuroImage,
Gospodarce i Ochronie Srodowiska, vol. 10, no. 3, pp. 26–31, 2020. vol. 46, no. 1, pp. 64–72, 2009, doi: 10.1016/j.neuroimage.2009.02.006.
[44] X. Ding, X. Yue, R. Zheng, C. Bi, D. Li, and G. Yao, “Classifying major [64] S. Song, K. D. Miller, and L. F. Abbott, “Competitive Hebbian learning
depression patients and healthy controls using EEG, eye tracking and through spike-timing-dependent synaptic plasticity,” Nature Neurosci.,
galvanic skin response data,” J. Affect. Disorders, vol. 251, pp. 156–161, vol. 3, no. 9, pp. 919–926, Sep. 2000.
May 2019. [65] P. Dayan and L. F. Abbott, “Neurons and neural circuits,” in Theoretical
[45] A. Gramfort, “MEG and EEG data analysis with MNE- Neuroscience: Computational and Mathematical Modeling of Neural
Python,” Frontiers Neurosci., vol. 7, pp. 1–13, Jan. 2013, doi: Systems. Cambridge, MA, USA: MIT Press, ch. 5, 2001, pp. 153–166.
10.3389/fnins.2013.00267. [66] S. Hochreiter and J. Schmidhuber, “Long short-term memory,” Neural
[46] Y. LeCun, Y. Bengio, and G. Hinton, “Deep learning,” Nature, vol. 521, Comput., vol. 9, no. 8, pp. 1735–1780, Nov. 1997.
no. 7553, pp. 436–444, 2015. [67] N. Kasabov, Time-Space, Spiking Neural Networks and Brain-
[47] W. Wang et al., “Learning of spatiotemporal patterns in a spiking neural Inspired Artificial Intelligence. Heidelberg, Germany: Springer,
network with resistive switching synapses,” Sci. Adv., vol. 4, no. 9, 2019.
Sep. 2018, Art. no. eaat4752. [68] L. Schmaal et al., “Subcortical brain alterations in major depressive
[48] A. Taherkhani, A. Belatreche, Y. Li, G. Cosma, L. P. Maguire, and disorder: Findings from the ENIGMA major depressive disorder working
T. M. McGinnity, “A review of learning in biologically plausible spiking group,” Mol. Psychiatry, vol. 21, no. 6, pp. 806–812, Jun. 2016, doi:
neural networks,” Neural Netw., vol. 122, pp. 253–272, Feb. 2020. 10.1038/mp.2015.69.
[49] C. Teeter et al., “Generalized leaky integrate-and-fire models classify [69] B. Ay et al., “Automated depression detection using deep representation
multiple neuron types,” Nature Commun., vol. 9, no. 1, p. 709, and sequence learning with EEG signals,” J. Med. Syst., vol. 43, no. 7,
Feb. 2018. pp. 1–12, Jul. 2019.