Functional Connectivity of Prefrontal Cortex in Various Meditation Techniques – A Mini-Review

Abstract

Meditation is a practice of concentration and relaxation. In philosophical terms, it is a process of gaining self-consciousness. Although there is diversity in meditation (Mindfulness, compassion, transcendental, and focused attention meditation), interventions show that meditation practices improve prefrontal cortex (PFC) functions like cognition, self-awareness, attention, and memory and reduce psychological symptoms. These results are thought to be due to meditation increasing functional connections of different brain regions. We reviewed to show the functional connectivity of the prefrontal cortex in various meditation practices. We were viewed various neuroimaging interventions of functional connectivity associated with the prefrontal cortex and different brain areas during meditation techniques on healthy meditators compared with non-meditators. fMRI findings show that meditation practices are associated with increased neural function and processing, default mode network, gray matter volume, and functional coupling in the brain area related to different parts of PFC. PFC's functional connectivity is associated with increased attention, working memory, cognitive control, executive control, emotion regulation, counteracting adverse effects, self-perception, and self-compassion. Furthermore, PFC's functional connectivity decreases anxiety, depression, perceived stress, negative emotion, and hyperarousal symptoms. In this review, we outlined the published effect of meditation on the function and structure of the different parts of the prefrontal cortex. We suggest a positive theoretical correlation between meditation and the functional connectivity of the prefrontal cortex. Altered prefrontal connectivity is seen in some neurological and psychosocial disorders. Therefore meditation can also play an influential role in treating these disorders.

Introduction

The human brain is a distributed network, but similar functional areas belong together by constantly sharing information. The prefrontal cortex (PFC) is the central structural region that contains executive functions such as planning, solving, working memory, cognition, and social control. It collects information from the environment and uses it intelligently to support thought processes, actions, and decisions. It manages emotions by inhibiting impaired thoughts, actions, and feelings.

In most cases of mental illness, PFC dysfunction is observed in cognitive and executive functions, including anxiety disorders, depression, schizophrenia, and addictive behaviors.[1] Disrupted connectivity is believed to be related to the spread of side effects and could also cause pathological diseases.[2]

Functional connectivity is characterized by the temporal dependence of neural activation schemes of different brain regions.[3] Improved brain connectivity, with all variations, is considered an evolutionary advantage mediated through complex sensorimotor functioning and complex cognitive abilities.[4]

Meditation is a mind–body practice that involves breath awareness, chanting mantras, and controlling thought processes. Meditation leads to a level of inner awareness and stillness.[5] Its philosophy and benefits are described in the oldest Indian texts, such as the Vedas, the Upanishads, the Bhagavad Gita (400600 BC), and the Yoga Sutras (900 BC).[6] In the Patanjali yoga sutra, two stages of meditation are explained, namely Dharana and Dhyana in Sanskrit “desabandhacittasya dharana” (Dharma PYS, Ch. 03, Verse 1), and “tatrapratyayaikatanata dhyanam” (Dhyana in Sanskrit; PYS, Ch. 03, Verse 2.[7] Dharna has focused attention meditation (FAM), and dhyana is effortless mental calmness or open monitoring meditation (OMM).

Different types of meditation affect different parts of the brain.[8] Zeidan et al. showed that mindfulness-mediated pain management was associated with greater activation in brain areas connected to pain's cognitive control, including the dorsolateral PFC (dlPFC), anterior cingulate cortex (ACC), and anterior insular cortex (AIC).[9] Dodich et al. found increased gray matter density due to 4-week Sahaj yoga meditation (SYM) and changes in the consistency of intrinsic cerebral activity in the right inferior frontal gyrus implying the dlPFC, posterolateral parietal areas.[10]

Independent of various meditations, little neuroimaging research has been done on meditation in the context of prefrontal activation and functional connectivity. The review presented helps describe PFC activation and functional connectivity in different types of meditation. In addition, this could be beneficial in generating the hypothesis for future meditation studies in clinical practice.

Methodology

The data were independently collected from two authors' articles available in PubMed from 2015. The search keywords were “mindfulness Meditation” AND “Open monitoring” AND “Compassion “AND “Prefrontal cortex.” The research was limited to human studies and articles published in English. Conference proceedings, editorials, comments, case reports, and books/chapters were not included. The results obtained were consolidated, and the duplicates were deleted [Figure 1]. The studies were then reviewed by reading the full texts of free available manuscripts, titles, and abstracts of paid articles. Studies that did not stratify the inclusion criteria were excluded [summary of Scientific studies presented in Table 1].

Figure 1.

Flowchart of the literature search and selection

Table 1.

Review studies’ summary

First Author	Study design and sample size	Type of meditation	Outcomes variables	Key findings
Kwak, 2020[11]	RCT n=67	Mindfulness	Attention network task MRI scan	Improvement in executive attention functions. Enhanced neural functions in the brain regions associated with alertness, attentional orientation, and conflict resolution regions of the anterior cingulated cortex and dorsolateral PFC
Allen[12]	RCT n=61	Mindfulness	Error awareness task assesses the meta-cognitive awareness, inhibition response, and executive functions fMRI task to assess the cognition by emotional interaction	Improved cognitive control and executive-related neural processing enhanced top-down resolution of response conflict and attentional improvements: The increased medial prefrontal cortex, insula, and anterior cingulate activity
Tang[13]	RCT n=60	Mindfulness	Smoking amount (carbon monoxide level) fMRI	Increased activity at anterior cingulated cortex and dorsolateral PFC, and inferior frontal gyrus/ventrolateral PFC. Decreased activity in the posterior cingulated cortex and cerebellum neural correlation with smoking reduction
Taren[14]	Single-blinded RCT; n=35	Mindfulness	High-resolution T1-weighted gradient-echo images fMRI	It increased resting-state functional connectivity
Creswell[15]	RCT; n=35	Mindfulness	IL-6, psychosocial measure, fMRI	The left dorsolateral PFC cluster increases resting-state functional connectivity with the posterior cingulate cortex
King[16]	RCT; n=63	Mindfulness	Emotion regulation tasks fMRI	Reduction in PTSD symptom severity Increased default mode network with dorsolateral prefrontal cortex regions and dorsal ACC
Mahone[17]	Within-group design; n=16	Transcendental	fMRI	Activation in the bilateral anterior cingulate gyrus and bilateral dorsolateral PFC and areas of deactivation in the pons and cerebellum
Weng[18]	RCT; n=43	Compassion	fMRI altruistic behavior task	Activation in regions implicated in social cognition and emotion regulation, including the inferior parietal cortex and dorsolateral PFC
Lee[19]	RCT; n=22	Focused-attention meditation	fMRI task (continuous performance task and emotion performance task)	More vital interaction of fMRI signals in attention-related regions
Leung[20]	RCT; n=25	Loving-kindness meditation	MRI	More gray matter volume was detected in the right angular gyrus, and the right posterior parahippocampal gyrus’s left temporal lobe
Yamaya[21]	RCT; n=44	Focused attention meditation	fNIRS images	Results showed enhanced bilateral dorsolateral PFC activation
Yang[22]	Longitudinal design n=13	Mindfulness	Profile of Mood States, Epidemiologic Studies Depression Scale, The State-Trait Anxiety Inventory, fMRI	The outcome showed a decrease in depression and anxiety scores. During meditation, the internal consistency in the precuneus and the temporoparietal junction increased, and frontal brain regions decreased
Mascaro[23]	RCT; n=21	Compassion meditation	fMRI Emotion and gender task Reading the mind in the eyes task	Enhanced empathic accuracy-related brain activity Increased neural activity in the inferior frontal gyrus and dorsomedial PFC
Do11[24]	Pre-post design without control	Mindfulness	fMRI Expectation and negative emotion task	Results showed a reduction in amygdala activation associated with emotion regulation. Emotion-related functional connectivity between the amygdala and left dorsal PFC was increased during mindfulness
Laneri[25]	RCT n=51	Mindfulness	fMRI Interpersonal Reactivity Scale Compassionate Love Scale	Increased activations of the anterior cingulated cortex and the left anterior insulate. Activations of the caudate nucleus and a region within the thalamus/brainstem
Farb[26]	RCT n=20	Mindfulness	fMRI Breath monitoring task, cognitive suppression task working memory maintenance task	Greater interoceptive attention-related activation in the right sensorimotor cortex and posterior insula. Interoceptive attention-specific functional plasticity in the middle and anterior insula
Kral[27]	RCT n=158	Mindfulness	fMRI Emotion regulation task Five Facet Mindfulness Questionnaire	Increased functional connectivity between the amygdala and the ventromedial prefrontal cortex. Results also showed affective responding through reduced amygdala reactivity and heightened amygdale ventromedial prefrontal cortex connectivity
Lenhart[28]	Pre-post design without control n=27	Focused attention meditation	Health-related quality of life STADI MRI	Reduced gray matter density in the right medial PFC, the lateral parietal and temporal cortex
Chételat[29]	RCT with Cohort pilot study; n=192	Meditation	MRI and FDG-PET scans Self-perceived sleep quality Glucose metabolism	Results showed higher gray matter volume and glucose metabolism in the anterior cingulate and ventromedial PFC, insula, temporoparietal junction, and posterior cingulate cortex
Hernández[30]	RCT; n=46	Sahaj yoga meditation	MRI	Increased functional connectivity of medial PFC with bilateral anterior insula/putamen is essential for interoception, emotion, and attention
Lutz[31]	RCT; n=44	Mindfulness	fMRI Five Facets Mindfulness Questionnaire	Activation in the dorsomedial PFC decreased functional connectivity to the posterior midline and parietal regions
Sevinc[32]	RCT; n=60	Mindfulness	MRI Various structured questionnaires	Increased functional connectivity of ventromedial PFC to a cluster in the frontopolar cortex. Increased Functional connectivity of ventromedial PFC to the supplementary motor area potentially shows the present moment awareness and focused attention. Significant functional connectivity of the right anterior insula
Jang[33]	RCT; n=68	Brain-wave vibration meditation	fMRI The Beck Depression Inventory the Beck Anxiety Inventory	Meditation practitioners demonstrated greater functional connectivity within the DMN in the medial PFC area

RCT=Randomized controlled trial, MRI=Magnetic resonance imaging, fMRI=Functional MRI, PFC=Prefrontal cortex, IL-6=Interleukin-6, PTSD=Posttraumatic stress disorder, STADI=State-Trait Anxiety Inventory, ACC=Anterior cingulate cortex, fNIRS=Functional near-infrared spectroscopy, DMN=Default mode network, FDG= Fluorodeoxyglucose PET= Positron Emission Tomography

We included studies of changes in brain structure and function observed through meditation. Studies must have meditation or aspects of the program as the intervention and functional and structural magnetic resonance imaging (MRI) as the imaging modality. There was no age range, health status, or ethnicity restrictions. Our main goal is to examine studies that report an activation, deactivation or functional connectivity, or structural changes of PFC due to meditation. Since the spatial resolution of electroencephalography is lower, we have limited the imaging method to functional MRI (FMRI). Unpublished dissertations and conference papers were not considered.

Results

The initial database (PubMed) search indicated 66 potentially eligible articles [Figure 1]. Of these, 43 articles were excluded as they did not meet our review objective.

Activation of the lateral region of prefrontal cortex in different styles of meditation

The PFC is the part of the cerebral cortex overlying the anterior frontal lobe. It is divided into lateral, medial, and inferior regions. The lateral area of the PFC is further divided into dlPFC and ventrolateral (vlPFC). dlPFC extends between the brain's upward longitudinal cleft and downward lateral cleft on the lateral side of the brain and also collects input from the motor cortex, from the temporoparietal junction. The dlPFC and vlPFC are involved in the functioning of attention, decision-making, working memory, and cognitive control.[34] The orbitofrontal cortex (OFC) comprises the inferior surface of the PFC. The functional anatomy of the prefrontal cortex is presented in Figure 2 and functional connectivity of the prefrontal cortex is presented in Figure 3.

Figure 2.

Functional anatomy of prefrontal cortex. Source: Biorender.com

Figure 3.

Functional connectivity of prefrontal cortex. Source: Biorender.com

A randomized controlled trial (RCT) performed by Kwak et al. was conducted to assess the effect of a 4-day meditation on the attentional network. Twenty-three experimental groups in meditation practice and 14 control groups in a relaxing retreat group will undergo attention network testing while fMRI imaging is performed before and after the intervention. The experimental group found activation in dlPFC and the ACC.[11] In another study of cognitive, affective neural plasticity conducted by Allen et al., there is greater activation in dlPFC.[12] Tang et al. investigated that meditation might reduce smoking, and fMRI scans increased activity in dlPFC and ACC, brain areas associated with self-control in the meditation group.[13] Taren et al. illustrate the increased functional connectivity of the left dlPFC with the right inferior frontal gyrus, right middle frontal gyrus, right supplementary eye field, right parietal cortex, and left middle temporal gyrus after meditation, brain areas associated with relaxation control.[14]

Similarly, researchers reported increased functional connectivity with the left dlPFC and the posterior cingulate gyrus.[15] King et al. concluded that mindfulness meditation could improve the ability to shift attention. Results showed increased functional connectivity between the default mode and executive network posts. It has also been associated with reducing symptoms of posttraumatic disorders supporting the adjuvant therapeutic use of mindfulness-based therapies.[16] Mahone et al. found that blood flow patterns in the ACC and dlPFC were significantly increased and decreased in the pons and cerebellum while performing transcendental meditation.[17] Weng et al. showed that compassion meditation (CM) is associated with altered activation in the lower parietal cortex and dlPFC. CM increases dlPFC connectivity with the nucleus accumbens.[18] Weng et al. showed that CM was connected with altered activation in brain regions associated with social cognition and emotion regulation, including functional connectivity of dlPFC with the nucleus accumbens; this suggests that the idea of compassion might be generated through meditation training.[18] Another study showed that top-down attentional control activates bilateral dlPFC, increasing meditators' working memory capacity.[21] Mascaro et al. conducted a RCT in which they found increased neural activity in the inferior frontal gyrus and dlPFC after meditation.[23] Yang et al. observed mindfulness meditation-induced neuroplasticity of affective disorders such as depression after 40 days.[22] Mahone et al. found that blood flow patterns during transcendental meditation were higher in the ACC and dlPFC.[17]

Activation of the medial region of prefrontal cortex in different styles of meditation

The medial region of the PFC is divided into dorsomedial (dmPFC) and ventromedial (vmPFC). The dorsomedial component of the PFC lies within an arc that extends downward from the supplementary motor area to the orbital component of the PFC. It is thought that the role of dmPFC is to engage in introspections. It is active in reflecting on the intentions and consequences of actions and in forgiving the transgressions of others.[35] It is speculated that this activity could also modulate stimulus-driven amygdala activity.[36] The dmPFC also responds to interoceptive and exteroceptive stimuli, particularly those encountered in social situations. The dmPFC is activated during the perception of pain in oneself and others. Doll et al. studied the effects of mindfulness on breathing in 26 healthy volunteers for 2 weeks and proposed that dmPFC activations are associated with mindfulness meditation. Furthermore, they found that emotional and functional connectivity between the amygdala and the left dmPFC was increased during mindfulness-on-breath meditation.[24] Laneri D results show increased activations of the anterior insula and cingulate gyrus as well as the dmPFC and temporal pole after long-term mindfulness training.[25] The result of Farb et al. showed the decreased recruitment of the dmPFC during interactive attention in mindfulness meditation.[26] Lutz et al. observed activation in the dmPFC after mindfulness meditation compared to control participants, along with increased functional connectivity to the posterior midline and parietal areas.[31]

vmPFC is located below dmPFC. A key difference to the dmPFC is that the vmPFC receives input from all sensory modalities. It has connections with the ACC, AIC, amygdala, and nucleus accumbens. These structures identify the valence and emotional tone of interoceptive and exteroceptive stimuli. Based on the nature of vmPFC's connections, it modulates social and personal decision-making. Kral et al. Observed short-term meditation practice results in increased functional connectivity between the amygdala and vmPFC during affective imagery, lowering amygdala reactivity to positive imagery than control.[27] Gray matter volume increased significantly in older experienced mediators in the bilateral vmPFC and ACC, insula, temporoparietal junction, and posterior cingulate cortex (PCC) compared to controls.[29] Gray matter volume in vmPFC, including rostral ACC, was increased after SYM. They further demonstrated increased functional connectivity between this area and putamen and decreased functional connectivity with the right thalamus/parahippocampal gyrus while performing the meditation.[30] Lenhart et al. showed reduced gray matter in the right dmPFC.[28]

Activation of the lower region of the orbitofrontal cortex in different meditation

The OFC is defined as the ventral surface of the frontal lobe from the rectus gyrus on the ventral surface to the ventrolateral convexity lateral and from the limen of the insula posterior to the frontal pole. The OFC receives input from the temporal association cortex, the amygdala, and the hypothalamus, making it the highest integration center for emotional processing. It is involved in processing visceromotor states and calculating expected value, reward outcome, and subjectively experienced pleasure.[33] Zeidan observed that mindfulness-based pain relief was associated with greater activation in brain regions associated with cognitive alteration of pain, including OFC and AIC.[9] An fMRI study demonstrated the effect of meditation on relaxing the mind in major depressive disorders, showing increased functional connectivity from the right dl to the left OFC.[37] Meditators who practiced mindfulness of their bodily sensations and emotions showed increased connectivity with the OFC/vmPFC as controls. This area of the brain is strongly connected to limbic regions.

Sevinc et al. observed neural activity after mindfulness meditation. The results showed increased functional connectivity of the right inferior frontal gyrus, a key hub of intentional inhibition and control – with additional motor areas. Mindfulness meditation was associated with a significant increase in right anterior insula functional connectivity – an important hub of sensory perception and emphasis compared to control.[32] An RCT showed improved competency-related behavior and performance on attentional tasks in focused-attention meditators. After the affective image task, the activated regions in meditators were consistent with attention-related processing.

In contrast, control responses were more consistent with the distinction between emotional contagion and compassion/emotional regulation processes.[19] Leung et al. found significantly increased gray matter volume in the right angle and the posterior hippocampal gyri in loving-kindness meditators.[20] The mediators demonstrated superior functional connectivity between the posterior cingulate and left inferior frontal gyrus while performing loving-kindness meditation. These results demonstrate that loving-kindness meditation is associated with a present-centered, selfless focus.

The studies informing functional connectivity and any other effect of PFC following meditation are summarized in Table 2.

Table 2.

The reported effects of meditation on the various area of prefrontal cortex

Dorsolateral PFC	Dorsomedial PFC	Ventromedial PFC	OFC
Increased neural functions association with the right ACC and DLPFC; increased functional connectivity of left DLPFC to the right middle frontal gyrus	Reduction in depressive symptoms with involvement of the temporoparietal junction and its connectivity to ACC Emotion-related functional connectivity between amygdala and left dorsomedial PFC suggests amygdala-dorsal PFC integration as a potential neural pathway of emotion regulation Meditation practice also altered functional connectivity between the dorsomedial PFC and the posterior insula	Meditation may improve affective responding (reductions in reactivity to negative stimuli) through reduced amygdala reactivity, and raised amygdala - Ventromedial PFC connectivity during affective stimuli. Participants practicing short-term meditation demonstrated gray matter decreases in extended parietotemporal regions, the ventromedial PFC. The same participants reported significant lower levels of anxiety and increased levels of psychological well-being after meditation	In a study, default mode network showed increased connectivity to the OFC in meditators. This area of the brain has been implicated in processing visceromotor states, as well as in computing expected value, reward outcome, and subjectively experienced pleasure

DLPFC=Dorsolateral prefrontal cortex, ACC=Anterior cingulated cortex, PFC=Prefrontal cortex, OFC=Orbitofrontal cortex

Discussion

In this review, we have outlined the published effect of meditation on the function and structure of the various parts of the PFC and its connection. The recent trend evident among the research studies reviewed was in favor of various meditations associated with the functional connectivity and activity of the PFC.

The circuits involved in the different styles of meditation are the default mode network (DMN), the salience network (SN), and the central executive network (CEN). The DMN refers to an interconnected group of brain structures, including the vmPFC, PCC, and precuneus.[33] The important connection of the DMN is the hippocampus and the amygdala. Increased activity of the DMN can be observed in mind wandering state.[16] Our finding showed that FAM activates the dlPFC and deactivates the vmPFC. The SN, which has hub nodes in the ACC and anterior insula, responds to socially salient events, integrates autonomic and emotional information, and aids in reward processing.[38] Centered in the dlPFC and the posterior parietal cortex, CEN deals with cognitively demanding mental activity and working memory.[39] FAM activates connectivity between the dlPFC and the posterior parietal cortex.

Instead of drawing attention to objects, just keep your mind open and observe all aspects of our experience (albeit emotions and body awareness) without judgment or attachment, called OMM. Our analysis showed that the neuronal activity of PFC in OMM differs from FAM. FAM is associated with increased dlPFC activity and connectivity in the ACC and right insula compared to OMM. ACC is known as the primary limbic cortex and the cingulate cortex's affective or emotional division. It monitors amygdala sensory stimuli and plays an essential role in the network related to alternation, orientation, and execution function.[40] Coactivator of frontal and parietal and ACC in response to tasks known to activate the cingulate-frontal-parietal network that supports motivation, attention, motor control, and reward processes in healthy individuals. The insular cortex lies deep in the lateral cleft of the cerebral cortex and, together with ACC, is responsible for switching between DMN and SN. Various studies suggest that the maladaptive functional connectivity of the cingulate frontal-parietal network triggers the pathophysiology of psychiatric disorders, for example, altered functional connectivity in the dlPFC, PFC hippocampus, and amygdala pathways in patients with schizophrenia, bipolar disorder, and depression.[41,42] Many studies have shown that patients with psychiatric disorders have cognitive dysfunctions such as cognitive flexibility[43] and working memory,[44] due to PFC functional connectivity malfunctions. FAM can also be an effective treatment for these disorders. FAM increases functional connectivity and activation of PFC regions and heightens alertness,[45] visuospatial processing,[9] and working memory,[46] and cognitive flexibility.[47] Therefore, considering the recent evidence that increased DMN activity is associated with negative psychological consequences, regular practice of FMA will be the meditation of choice for psychiatric disorders.

Autographic memory is a memory system consisting of episodes retrieved from a person's life based on a combination of episodic or event experiences. The neural core network consists of the left vmPFC and vlPFC, the temporoparietal junction, and the PCC cortex.[48] Our result showed that OMM improved the ability to detach from experiences such as autobiographical memories compared to FAM. The PCC is the part of the brain involved in referential processing, including past and future thinking.[49] Therefore, given recent evidence, regular practice of OMM will disable the neural network of autograph memory.

CM involves cultivating positive emotions such as joy and compassion. FAM showed less emotional reactivity and more activity in the left insula when seeing a happy image and more activity in the inferior and superior frontal gyrus when seeing a sad image. At the same time, CM increased activity in the left ACC and right inferior frontal gyrus in a happy image and higher activity in the left caudate nucleus and medial frontal gyrus. CM experts linking the negative/sad image showed brain activity associated with heightened emotional reactivity and more voluntary emotion regulation. Future studies should focus on meditation training interventions and standard treatments for integration.

Neurobiological improvements are associated with cognition and increased gray matter volume in expert meditation professionals.[29] Therefore, meditation can be an adjunctive treatment to improve gray matter volume and counteract cognitive dysfunction. Impaired cognitive function in individuals affected by Parkinson's disease can be attributed to a reduced hippocampus volume.[50] Meditation practice can play a therapeutic role alongside standard therapy in treating Parkinson's disease, as meditation improves bilateral hippocampal volume.

Conclusion

The different styles of meditation can alter the functional activity and connectivity of the PFC region, which is associated with increased attentional function, working memory, cognitive control, executive control, emotion regulation, countering negative effects, self-awareness, and compassion. The overall increase in functional connectivity and activity of the PFC may explain the decrease in anxiety, depression, perceived stress, negative emotions, and hyperarousal symptoms in meditators. An increase in mindfulness, alertness, and awareness has been demonstrated following meditation training programs, and this positive result can be extrapolated to a clinical population.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.