Spectral dynamics of electroencephalographic rhythms during verbal learning: analysis of the Rey test stages

Shlyakhov Ivan Sergeevich ORCID: 0000-0001-7801-382X Assistant; Department of Psychology; V.A. Almazov National Medical Research Center Postgraduate student; Faculty of Psychology; Saint Petersburg State University 199225, Russia, St. Petersburg, Vasileostrovsky district, Vadim Shefner str., 14, room 1, building 1 i.shlyakhov@spbu.ru Other publications by this author     Gorbunov Ivan Anatol'evich ORCID: 0000-0002-7558-750X PhD in Psychology Senior Lecturer; Faculty of Psychology; Saint Petersburg State University 199178, Russia, St. Petersburg, Vasileostrovsky district, line 8-ya.O., 77 i.a.gorbunov@spbu.ru

Tihonova Kseniya Aleksandrovna ORCID: 0009-0002-0148-7298 Student; Institute of Medical Education; V.A. Almazov National Medical Research Center 134 Engels Ave., St. Petersburg, 194356, Russia, 3 letters A ksenia.tih@mail.ru

Introduction

The study of the spectral dynamics of an electroencephalogram (EEG) in performing verbal learning tasks is an important area of modern neuroscience. The growing interest in the neurophysiological foundations of memory and cognitive control is due not only to academic interest, but also to applied tasks to identify markers of cognitive impairment, as well as the creation of neuro-rehabilitation programs.

Despite the abundance of research on the Rey Auditory Verbal Learning Test (RAVLT) and memory in general, the topographic organization of EEG rhythms in the dynamics of all phases of the Rey test is still poorly understood. In particular, spectral changes at all key stages of this technique have not been systematically analyzed. The purpose of this study is to identify and characterize the dynamics of spectral changes in the EEG at various stages of the Ray verbal learning test.

The data obtained will expand the understanding of the functional role of cortical rhythms and the topical organization of cognitive functions in performing complex mnestic tasks.

Research objectives:

1. Analyze spectral power in the delta, theta, alpha, beta, and gamma ranges when performing different Ray test samples;

2. Compare the topographic power distributions between the stages: memorization, interference, immediate and delayed reproduction of stimuli;

3. To identify neurophysiological correlates of the processes of memorization, reproduction and overcoming interference.

According to the systemic concept of memory, the processes of consolidation and reconsolidation are interpreted as inseparable aspects of the formation of individual experience. They are not limited to the stabilization of the footprint, but include the restructuring of previously formed systems under the influence of new behavioral acts ^[1]. This position is especially relevant in the context of the multi-stage RAVLT test, where memory is subjected to both reinforcement (memorization) and modifying effects (interference), as well as subsequent actualization (reproduction).

Short-term memory (KP) is a limited capacity of the cognitive system for simultaneous retention and processing of information, which averages 7± 2 units of perception. KP is characterized by the preservation of information, relying mainly on the external physical characteristics of stimuli. When the volume of perception is exceeded, subjective organization of the material occurs, for example, systematization or grouping of elements to optimize memorization ^[2].

KP acts as a key link in the information processing system, providing temporary storage and primary processing of data before transferring them to long-term memory. It acts as a "cognitive filter", selecting the most significant data through the mechanisms of attention ^[3].

The formation of short-term memory is associated with the synchronization of theta and gamma rhythms between the hippocampus, amygdala, and neocortex in the parietotemporal regions. Disruption of synchronization between these structures leads to a decrease in the efficiency of short-term reproduction, which emphasizes the role of theta rhythm in the implementation of the CP process as the neurophysiological basis for short-term memorization and updating of information ^[4].

Interference is a cognitive phenomenon that occurs when two tasks are performed simultaneously, when the control of the main task involuntarily activates the execution of an additional one that must be ignored. This is due to the interaction of the processes of control over the correctness of execution and the selection of the relevant stimulus, which causes a cognitive conflict, leading to further errors. Interference is caused by the peculiarities of cognitive control, rather than limited attention. Its severity decreases with increasing complexity of the main task and increases with the similarity of the tasks performed, which emphasizes the role of associative connections and the emerging conflict between different tasks ^[5].

The alpha rhythm in the 10-12 Hz range is associated with the processes of semantic information processing. Increased alpha activity in the occipital, parietal, and frontal lobes serves as a predictor of the success of mnestic tasks, which indicates the functional significance of this neurophysiological marker in memory processes ^[6].

Alpha desynchronization in the parieto-occipital and frontal parts of the cerebral cortex can serve as a marker of information retention and processing in working memory ^[7].

On the other hand, Theta waves are markers of activation of incoming influences from the frontal cortex, and gamma waves are associated with the processes of encoding individual elements required for memorization, which subsequently leads them to combine into integral memories ^[8].

The Johnson E. study confirms the role of theta activity (4-7 Hz) in encoding and extracting episodic information. Synchronization of theta waves between the medial temporal lobe and the prefrontal cortex during the presentation of stimuli is associated with subsequent successful reproduction of the material. However, the theta rhythm also reflects the overall cognitive load, which complicates its interpretation as solely a marker of information assimilation ^[9].

Experimental data show that the process of assimilation and retention of information is accompanied by specific changes in cortical activity. An increase in the mnemonic load causes spectral changes in the theta and alpha ranges with topical specificity: the posterior cortex is activated during assimilation, and the frontal areas are activated during information retention. These data emphasize the involvement of the prefrontal cortex in mnestic processes ^[10].

With successful resolution of interference, there is a decrease in the power of theta activity in the anterior cingulate cortex, which serves as a neurophysiological marker of the effectiveness of the interference overcoming process and indicates the displacement of competing stimuli ^[11].

Synchronization of beta rhythms between the frontal and parietal regions of the brain accompanies improved performance in working memory tasks. An increase in the frequency and amplitude of beta oscillations is associated with an increased load on memory and information processing processes, and also correlates with individual differences in the success of the experimental task ^[12].

In addition, an increase in beta activity in the prefrontal cortex is observed at the end of the trial, when it is necessary to remove irrelevant information from working memory, which emphasizes the role of beta rhythm as a neurophysiological marker reflecting the process of controlling mnestic processes ^[13].

An increase in delta activity is observed mainly in the frontal cortex and anterior cingulate cortex, which indicates the involvement of these zones in the suppression of irrelevant stimuli, which contributes to focusing on the main task ^[14].

Methods:

The study involved 60 subjects aged 18 to 44 years. The participants had no history of neurological or psychiatric pathologies and did not take pharmacological drugs that could affect cognitive functions.

Two sets of words were used as experimental stimuli. Each of the sets included 15 words.

The participants were placed in a comfortable armchair in a soundproof room with dimmed lights. Detailed instructions were provided to the participants before each stage.

Ray's verbal learning test was used as an experimental technique. RAVLT is a classic test for evaluating auditory-verbal (verbal) memory and memorization processes ^[15].

Studies of the RAVLT structure have revealed its multicomponence, reflecting the differentiation of verbal memory into independent cognitive processes ^[16].

The first phase of the test involves learning and systematization of information. It is carried out with the help of progressive memorization upon repeated presentation of stimuli.

The stage includes five consecutive presentations of A list of words (samples 1-5), where active memorization occurs through semantic processing and the formation of associative connections in the hippocampus and medial temporal lobes ^[4]. The total reproduction rate (attempt 1– attempt 5) reflects the amount of immediate memory and attention stability, whereas the volume of the first reproduction characterizes short-term memory.

After the learning stage, the subjects are offered to memorize a list of B words of 15 words, the words in which are in no way related to the list of A words.

Babiloni C. In his study, he notes that after the interference list B, the memorization process stabilizes, associated with the movement of information from the hippocampal structures to the cortical regions ^[4]. Retroactive interference (the difference between the fifth attempt and the seventh attempt) demonstrates resistance to the interfering effects of new information.

At the stage of delayed playback, the subjects' long-term memory is evaluated.

RAVLT serves as a tool for the differential diagnosis of cognitive deficits, allowing us to explore the process of learning, retention, and information retrieval. ^[17]

The study consisted of successive stages. At the first stage, the subject was presented with the first set of 15 unrelated nouns (list A). Next, list A was read out five times in a row, after each presentation, the participant reproduced the maximum possible number of words (samples 1-5). Then a second, interfering list of 15 words (list B) was presented, which also had to be reproduced (sample 6). After that, the subject repeated the words from the first list (sample 7). After 20 minutes, delayed playback of words from list A was performed (sample 8).

An electroencephalogram (EEG) was recorded during the playback of the words. The EEG was recorded using 19 channels in a monopolar lead. The recording was carried out using a Micar 202 encephalograph with the placement of electrodes according to the 10-20 system. EEG processing was performed in the Python environment using the MNE-Python, SciPy, and StatsModels libraries. The raw data was band–filtered in the range of 0.5-45 Hz.

The Welch method using the Hanna window was used to evaluate the spectral characteristics of the power. The power spectral density (PSD) was calculated separately for each channel. Relative and logarithmic powers were calculated based on PSD in the following standard ranges: delta (0.5–4 Hz), theta (4-8 Hz), alpha (8-13 Hz), low beta (13-20 Hz), high beta (20-30 Hz), gamma (30-45 Hz). Relative power was calculated as the proportion of power in a given range of total power using logarithm.

The power differences between the stages of the Ray verbal test (samples 1, 5, 6, 7, and 8) were analyzed using single-factor variance analysis with repeated measurements (RM-ANOVA) for each channel–range combination. In the case of a statistically significant ANOVA effect (p < 0.05), the Hill correction for multiple comparisons was applied. All comparisons were carried out at the significance level α = 0.05.

Topographic power distributions and statistical significance were also visualized using topographic maps displaying logarithmic power and levels of p-values obtained by pairwise comparisons.

Results

Figure 1 Topograms of the power differences of the low-frequency beta rhythm (left) and delta rhythm (right).

A comparison of the first and fifth RAVLT attempts revealed a change in the power of rhythms in several ranges and leads. In the delta range, power decreased in the right frontal lead and in the right central lead (RM-ANOVA: F(4, 220) = 3.62, p = 0.007 Holm F4: p = 0.014; Holm C4: p = 0.003) (Fig.1). In the alpha range, the power increased in the central frontal lead (Channel Fz; RM-ANOVA: F(4, 220) = 5.86, p = 0.001; Holm: p = 0.026). In the low-frequency beta range, power increased in the right frontal and right central leads (RM-ANOVA: F(4, 220) = 3.62, p = 0.007; Holm F4: p = 0.043; Holm C4: p = 0.014) (Fig.1). In the high-frequency beta range, an increase in power was noted in the right central lead (Channel C4; RM-ANOVA: F(4, 220) = 3.53, p = 0.008; Holm: p = 0.026).

Figure 2. Topograms of power differences (1 sample vs 6 sample) of alpha rhythm (left) and delta rhythm (right).

Comparing the first and sixth RAVLT attempts, desynchronization of the delta rhythm was found in the left and right central leads (RM-ANOVA: F(4, 220) = 3.88, p = 0.005; Holm C3: p = 0.018; Holm C4: p = 0.045) (Fig.2). Synchronization was also noted alpha rhythms in the frontal, central, parietal, and right temporal leads (RM-ANOVA: F(4, 220) = 2.89, p = 0.023; Holm F3: p = 0.023; Holm C3: p = 0.044; Holm C4: p = 0.023; Holm P4: p = 0.009; Holm P8: p = 0.015; Holm Fz: p = 0.001; Holm Cz: p = 0.027; Holm Pz: p = 0.003) (Fig.2). Statistically significant differences were found indicating synchronization of the low-frequency beta rhythm in the right central lead and the left temporal lead (RM-ANOVA: F(4, 220) = 5.04, p < 0.001; Holm C4: p = 0.029; Holm T7: p = 0.025).

Figure 3. Topograms of power differences (1 sample vs 7 sample) of alpha rhythm (left) and delta rhythm (right).

Figure 4. Topograms of power differences (1 sample vs 7 sample) of the low-frequency beta rhythm (left).

A comparison of the first and seventh RAVLT attempts revealed desynchronization of the delta rhythm in the right frontal, left central, and right temporo-occipital leads (RM-ANOVA: F(4, 220) = 3.62, p = 0.007; Holm F4: p = 0.025; Holm C3: p = 0.014; Holm T8: p = 0.039) (Fig.3). Statistical analysis revealed statistically significant differences indicating alpha rhythm synchronization in the frontal, central, temporal, and central parietal leads (RM-ANOVA: F(4, 220) = 3.81, p = 0.005; Holm F4: p = 0.022; Holm C3: p = 0.033; Holm T7: p = 0.025; Holm T8: p = 0.005; Holm Fz: p = 0.001; Holm Cz: p = 0.025; Holm Pz: p = 0.004) (Fig.3). Synchronization of the low-frequency beta rhythm in the frontal, left occipital and central leads was also noted (RM-ANOVA: F(4, 220) = 3.00, p = 0.019; Holm Fp1: p = 0.046; Holm Fp2: p = 0.030; Holm F4: p = 0.018; Holm C3: p = 0.013; Holm C4: p = 0.029; Holm O1: p = 0.018; Holm F8: p = 0.025; Holm T7: p = 0.054; Holm T8: p = 0.008) (Fig. 4).

Figure 5. Topograms of power differences (1 sample vs 8 sample) of the alpha rhythm (left) and the low-frequency beta rhythm (right).

Comparing the first and eighth RAVLT attempts revealed desynchronization of the delta rhythm in the right central lead (Channel C4; RM-ANOVA: F(4, 220) = 4.98, p <0.001; Holm: p = 0.006) and alpha rhythm synchronization in the frontal and central leads (RM-ANOVA: F(4, 220) = 3.81, p = 0.005; Holm F4: p = 0.025; Holm C3: p = 0.033; Holm C4: p = 0.025; Holm Fz: p = 0.015) (Fig.5). Synchronization of the low-frequency beta rhythm was also noted in the right parietal lead (Channel P4; RM-ANOVA: F(4, 220) = 3.42, p = 0.010; Holm: p = 0.013) and the right central lead (Channel C4; RM-ANOVA: F(4, 220) = 5.04, p <0.001; Holm: p = 0.016) (Fig.5). Synchronization of the high-frequency beta rhythm in the right central lead was also observed (Channel C4; RM-ANOVA: F(4, 220) = 3.53, p = 0.008; Holm: p = 0.048).

A comparison of the fifth and seventh RAVLT attempts revealed desynchronization of the delta rhythm in the left temporal lead T8 (RM-ANOVA: F(4, 220) = 2.84, p = 0.025; Holm T8: p = 0.039), as well as synchronization of the low-frequency beta rhythm in the left occipital lead O1 (RM-ANOVA: F(4, 220) = 3.60, p = 0.007; Holm O1: p = 0.031). Comparison of the seventh and eighth RAVLT attempts revealed desynchronization of the theta rhythm in the central frontal lead Fz (RM-ANOVA: F(4, 220) = 2.68, p = 0.033; Holm Fz: p = 0.009).

Discussion of the results

The results obtained demonstrate the specific dynamics of spectral EEG changes at various stages of the Ray verbal learning test, which makes it possible to clarify the neurophysiological mechanisms underlying short-term and long-term memorization, as well as the processes of interference and reproduction.

At the stage of active learning (samples 1-5), an increase in alpha and beta activity was observed in the central and frontal leads, which is consistent with the data on the involvement of these rhythms in the processes of semantic processing of the material ^[17]. An increase in the low-frequency and high-frequency beta rhythm in the right frontal and central zones may indicate an increasing cognitive load and activation of executive functions that control information retention and processing ^[6],[13]. A decrease in delta activity in the right frontal and central leads reflects a weakening of focus on the task ^[14].

The appearance of desynchronization of the delta rhythm and synchronization of alpha and beta activity upon presentation of the interference list (sample 6) indicates the actualization of the processes of cognitive control and suppression of irrelevant information. These changes may reflect an attempt to suppress previously learned material and redistribute cognitive resources for processing new information, which is consistent with models of retroactive interference ^[5],[11].

The return to the reproduction of the original list (sample 7) was accompanied by significant alpha synchronization in a wide topographic range (frontal, central, temporal, and parieto-occipital regions), which may be associated with the activation of mechanisms for searching and updating previously encoded information ^[6]. Concomitant synchronization of the beta rhythm indicates the involvement of arbitrary control, which helps to overcome interference ^[12].

At the stage of delayed reproduction (sample 8), pronounced alpha and beta synchronization persists, mainly in the frontal, central and right parietal-occipital leads. Thus, the synchronization of these rhythms can be a marker visualizing the actualization of the mechanisms of long-term storage and updating of information.

It should also be noted the role of theta rhythm desynchronization in the central frontal region when comparing the seventh and eighth samples. This may indicate a decrease in cognitive load after successful actualization of memories during word reproduction on the seventh test ^[9].

Conclusion

The stages of Ray's verbal learning test reflect not so much isolated acts of memorization as successive phases of formation, modification, and integration of functional systems. The initial presentation of List A initiates systemogenesis, the formation of a new neural organization associated with memorizing material. Repeated presentations contribute to systemic consolidation, during which the new system is strengthened and integrated into the previously existing structure of experience, which is accompanied by an increase in the reproduction of learned stimuli and stabilization of cognitive activity ^[1]. These stages were accompanied by increased alpha and beta activity in the frontal and central leads, reflecting active semantic processing and increasing cognitive load. ^[6],[12]

The presentation of the interfering list B triggers the mechanism of accommodative reconsolidation. Thus, the previously formed system is undergoing restructuring under the influence of new information. The return to the original list and the reproduction of stimuli after a break reflect the stability and flexibility of memory as a systemic education. These stages demonstrate the ability of an already modified system to be updated again, as well as the effectiveness of reconciling old and new experiences. These stages were accompanied by desynchronization of low-frequency rhythms and synchronization of alpha and low-frequency beta rhythms. These markers may indicate the activation of arbitrary control mechanisms, resulting in the successful overcoming of the interference effects of List B. ^[11],[13]

The data obtained confirm the existing theoretical ideas about the neurophysiological mechanisms of various types of memory and interference, and also expand them, pointing to the dynamic and topical restructuring of cortical activity depending on the stage of RAVLT. Spectral analysis of the EEG revealed the significant role of alpha and beta rhythms in the function of voluntary attention, encoding and updating information, as well as the participation of low-frequency rhythms in the processes of suppression of irrelevant stimuli and regulation of cognitive load. The data obtained complement the understanding of the spectral organization of cognitive activity and can be used as diagnostic indicators of the state of verbal memory, as well as for the development of neuro-rehabilitation programs for the correction of cognitive impairments.