The relationship between the brain oscillations and WM capacity has been investigated in the different brain regions (parietal, frontal, occipital regions, hippocampus…etc.), and several studies have focused on the association between CFC, particularly theta-gamma coupling (TGC), and WM performance (Schack et al., 2002; Demiralp et al., 2007; Mizuhara and Yamaguchi, 2011; Bahramisharif et al., 2018; Biel et al., 2021). Theta/gamma PAC is found in the hippocampus and other brain structures (Maris et al., 2011; Belluscio et al., 2012; van der Meij et al., 2012; Colgin, 2015) and provides a code for representing and maintaining the multiple WM items-theta/gamma neural codes (Axmacher et al., 2010; Lisman and Jensen, 2013). The theta/gamma neural code hypothesis posits that the conserved memory items are registered via theta-nested gamma cycles in the sensory regions. Accordingly, the theta-gamma neural code coordinates communication between the different brain cortices during memory and sensory processes (Lisman and Jensen, 2013) and is specifically correlated to the WM requirements (Park et al., 2013).

Several studies have used intracranial EEG data in patients with epilepsy along with the behavioral outcomes to demonstrate the association between theta/gamma CFC across different brain regions and WM performance (Canolty et al., 2006; Rizzuto et al., 2006; Axmacher et al., 2010; Freunberger et al., 2011; Chuderski, 2016; Chai et al., 2018). The results of these studies can be summarized as follows: theta/gamma PAC distributed across the cortex and the strength of TGC increased with more cognitively demanding WM tasks. Moreover, a significant effect was observed when the gamma oscillations were detected in the trough of theta cycles (Canolty et al., 2006). In general, the theta troughs and peaks have different functions: WM retrieval occurs during the peaks, whereas WM encoding occurs during the troughs (Rizzuto et al., 2006). Axmacher et al. found that the WM maintenance is associated with the TGC in the hippocampus and the modulation of beta/gamma amplitude and theta activity were associated with a relatively large number of WM items (Axmacher et al., 2010). On the other hand, Chaieb et al. observed theta and beta/gamma phase-phase coupling in the hippocampus during the maintenance of multiple WM items (Sternberg WM task) in pre-surgical patients with epilepsy (Chaieb et al., 2015). All these studies are summarized in Table 1.

Cross-frequency coupling supports the organization of brain rhythms and is present during a range of cognitive functions. However, little is known about whether and how long-range CFC across the distant brain regions subserves WM. Here we report that theta–slow gamma coupling between the hippocampus and medial prefrontal cortex (mPFC) is augmented in a genetic mouse model of cognitive dysfunction. This increased CFC is observed specifically when the mice successfully perform a spatial WM task. In wild-type mice, increasing task difficulty by introducing a long delay or by optogenetically interfering with encoding, also increases the theta–gamma coupling during correct trials. Finally, the epochs of high hippocampal theta–prefrontal slow gamma coupling are associated with the increased synchronization of neurons within the mPFC. These findings suggest that the enhancement of theta–slow gamma coupling reflects a compensatory mechanism to maintain spatial WM performance in the setting of increased difficulty. The association between WM and theta-gamma PAC in the frontal, parietal, occipital, and posterior cortices has been reported in several studies using the different tasks (pictorial recognition tasks, delayed match-to-sample visual WM task, verbal delayed match to sample task, delayed figure recall, n-back task, etc.) to demonstrate the association of interest by using the EEG recordings (Griesmayr et al., 2010; Holz et al., 2010; Park et al., 2011; Friese et al., 2013; Köster et al., 2014; Lee and Yang, 2014; Graetz et al., 2019; Tseng et al., 2019; Fernández et al., 2021). The lowest level of TGC coupling was found in the patients with Alzheimer's dementia, followed by the patients with MCI and finally healthy controls (Goodman et al., 2018). All the studies showed modulations in the theta-gamma CFC related to correctly identified/retrieved items. Besides that, a decrease in the prefrontal and occipital alpha oscillatory activities was observed by Friese et al. (2013). The details of the studies are summarized in Table 1. The combined effect of WM training and transcranial direct current stimulation (tDCS) on the behavioral changes was investigated using the EEG features and cognitive task scores, and it was found that an increase in PAC between the prefrontal theta oscillations and temporo-parietal gamma oscillations was associated with the improvement in behavioral task scores, and more prominent improvement was found when the gamma waves coincided near the theta peaks (Jones et al., 2020).

The theta/gamma PAC strength is influenced by the oscillatory activities of other frequency bands; alpha amplitude influenced TGC in the two intracranial electroencephalography (iEEG) experiments that used different WM tasks (Leszczyński et al., 2015). Sauseng et al. found that repetitive TMS at alpha frequency suppressed distracting information and could influence the STM capacity (Sauseng et al., 2009). On the other hand, delta-alpha coupling influenced TGC and supported switching between the WM modes in the hippocampal region (Leszczyński et al., 2015).

The default mode network (DMN) arises from the medial prefrontal cortex, the posterior cingulate cortex, and the inferior parietal cortex (Buckner et al., 2008). It is associated with episodic memory and self-referential thinking (Buckner et al., 2008; Knyazev et al., 2011; Weiler et al., 2014). The activity of DMN is higher during the resting state as compared with the task-performing state (Buckner et al., 2008). Indeed, an association between the DMN and WM networks has been suggested where DMN nodes could be activated during the memory phases (Hahn et al., 2007; Vilberg and Rugg, 2008; Daselaar et al., 2009). Moreover, the activity of DMN was mediated by alpha and beta oscillations, and the connectivity between some DMN parts is correlated to the alpha oscillatory activities (Hacker et al., 2017; Tang et al., 2017). A decrease in DMN functional connectivity and alpha power has been detected in patients with AD (Jeong, 2004; Zhang et al., 2009). In contrast to the young adults, old adults maintained synchronization in the resting state network and lacked the ability to synchronize the frontoparietal task-related network activities during the task performance (Pinal et al., 2015).

The electrophysiological studies have shown that when the content of WM changes from multiple items to distinct visual or spatial information, the oscillatory theta activities are replaced by alpha ones (Fries et al., 2001; Sauseng et al., 2005). Moreover, the studies examining the brain oscillations during the WM delay period found that the theta oscillatory activities occurred predominantly in the tasks that required sequential multiple WM item coding, while the alpha-oscillatory activities occurred in the tasks that required retention of visual or spatial information presented simultaneously (Roux and Uhlhaas, 2014). CFC between the parieto-occipital alpha activity and topographically distributed gamma activity is involved in prioritizing different visual representations in WM and deficits in the prefrontal cortex disrupt this process (Davoudi et al., 2021).

Alpha/gamma coupling has been demonstrated during visual WM maintenance in patients with epilepsy (Voytek et al., 2010). Park et al. used MEG data from healthy participants who were asked to recall the displayed images and found a reduction in the alpha power and an enhancement of alpha/gamma PAC during the process of recalling the images (Park et al., 2016). Moreover, alpha/beta and gamma power in the early visual cortex (in the dorsal and ventral visual streams) were modulated in response to the demands of the n-back task (Popov et al., 2018). The details of the studies are summarized in Table 1. Presumably, the theta and alpha activities are localized across different EEG recording sites. This assumption is supported by electrocorticography recordings, which showed that the alpha/gamma coupling was detected in the parietal–occipital cortices during the tasks requiring visual information processing, whereas theta/gamma PAC was predominantly observed in the frontotemporal regions during non-visual tasks (Voytek et al., 2010).

In principle, PAC can be generated in many ways; one source of the low-frequency band can be coupled to one or more sources of high-frequency bands. Thus, PAC is a general phenomenon and is not restricted to the theta/gamma frequencies. WM affects PAC in different ways; as WM could increase the PAC strength in some patterns and decrease it in others (Maris et al., 2011). CFC between the neural oscillations other than theta/gamma and alpha/gamma has been demonstrated during the WM maintenance as follows: (1) enhanced coupling between the theta/alpha phases and amplitude of beta has been demonstrated in temporal cortex during the visual delayed match-to-sample task (Daume et al., 2017a), (2) improved beta-theta PAC in the medial temporal lobe during the WM delay period (audio-visual delayed match to sample task) and enhanced phase synchronization between the medial temporal lobe and temporo-occipital areas in the beta band frequency range (Daume et al., 2017b), (3) improved the couplings between theta and alpha–gamma and between alpha and beta-gamma bands during the WM maintenance (delayed match-to-sample visual WM task) in the frontoparietal, dorsal, and visual areas (Siebenhühner et al., 2016), (4) increased alpha/theta phase synchrony was associated with the improved arithmetic task outcomes in the posterior and frontoparietal regions (Rodriguez-Larios and Alaerts, 2019), (5) the PAC (frontal theta phase and parieto-occipital alpha amplitude) strength decreased with increasing difficulty of both the correct and incorrect responses to the arithmetic tasks (Dimitriadis et al., 2016). The details of the studies are summarized in Table 1.

The non-invasive brain stimulation methods are a potent way to study the causal relationship between brain activities and behavioral outcomes. These methods could causally modulate the behavior using electric or magnetic fields (Walsh and Cowey, 2000; Miniussi and Ruzzoli, 2013). Several studies have investigated the effect of frequency-tuned tACS and TMS on the WM performance with mixed results (Jaušovec et al., 2014; Hoy et al., 2015; Chander et al., 2016; Alekseichuk et al., 2017; Kuhnke et al., 2017; Sreeraj et al., 2017; Borghini et al., 2018; Wolinski et al., 2018; Jones et al., 2019; Beynel et al., 2020; Kehler et al., 2020; Papazova et al., 2020) and others. In the context of WM and CFC, a study was conducted to demonstrate the direct causality between the CFC and WM performance, the interaction between theta and gamma bands in the prefrontal cortex was externally modulated by CFC tACS protocol (Alekseichuk et al., 2016). The volunteers were instructed to perform the tasks during the stimulation and were assigned into three groups: sham stimulation (first group), continuous single-frequency theta stimulation (second group), and CFC tACS between theta and gamma frequencies (third group). Based on the behavioral and EEG data, the positive effect of continuous low-frequency entrainment on the WM performance was canceled out by the synchronization of high gamma bursts with the troughs of theta cycles (Alekseichuk et al., 2016). In contrast, a significant improvement in the WM performance was found when high oscillations gamma bursts (80–100-Hz frequency range) were embedded in the peaks of theta cycles (Alekseichuk et al., 2016).