Dysfunction: disinhibition, apathy, poor integration of aversive interoceptive cues
ACC, anterior cingulate cortex; ADHD, attention-deficit/hyperactivity disorder; BPD, borderline personality disorder; GABA, gamma-aminobutyric acid; GAD, generalized anxiety disorder; MCI, mild cognitive impairment; MDD, major depressive disorder; OCD, obsessive compulsive disorder; PFC, prefrontal cortex; PTSD, posttraumatic stress disorder.
Volumetric changes following exercise training have been most consistently observed in the prefrontal cortex (PFC), subcortex, and mesial temporal brain structures ( 43 ), with the most consistent changes in the dentate gyrus ( 44 , 45 ). The mesial temporal lobe (MTL) is particularly vulnerable to neurodegenerative disease processes, such as Alzheimer’s disease, although exercise appears to increase volume in this brain region across both middle-aged and older adult samples ( 46 ). Moderate-intensity training in older adults, for example, increases hippocampal volume with dose-response improvements from 6 to 12 months, offsetting normative neurodegenerative changes (1–2% annually), without volumetric increases in other brain regions ( 47 ). In one of the few exercise trials collecting neuroimaging data from participants with depression, depressive symptoms improved in parallel with increased MTL volume and improved verbal memory, despite a 30% dropout rate and lack of a significant treatment group benefit ( 48 ).
While most randomized controlled trials (RCTs) have focused on MTL brain areas, white matter changes have also been reported, particularly in PFC and parietal lobe areas critical for SN and ECN function ( 43 ). In a one-year training intervention, Voss and colleagues ( 49 ) demonstrated improvements in microstructural parameters of white matter integrity in the PFC, paralleling improvements in MTL brain regions. Similarly, during a 10- to 12-year follow-up examination of participants in the LOOK-AHEAD diabetes trial, the lifestyle intervention group demonstrated an impressive 28% lower white matter hyperintensity volume, compared to only a 9% lower ventricle volume ( 50 ). We recently reported parallel results in a pilot study of adults with depression, in which aerobic exercise stabilized white matter hyperintensity progression following a 16-week treatment ( 51 ). Notably, preliminary evidence suggests similar improvements following resistance training, with participants exhibiting improvements in PFC white matter volume and executive functioning ( 52 ).
The effects of exercise training on connectivity changes extend studies of structural markers by elucidating their functional significance to underlying behavioral changes. Extant connectivity studies suggest critical influences impacting SN and ECN neurocircuitry, independent of volumetric changes in DMN brain structures. Acute exercise, for example, has been shown to enhance efficiency within the DMN and improve functional modulation between networks, as indicated by enhanced ability of SN and ECN brain regions to selectively and adaptively inhibit DMN functioning ( 53 ), with parallel improvements in behavioral markers of cognitive control ( 54 ). Several RCTs have suggested that exercise training may enhance connectivity in clinically important neurocircuitry ( 54 – 56 ), and some suggest that markers of brain connectivity hold central importance as translational biomarkers ( 55 ). Previous randomized trials of exercise training suggest that it may improve ECN and DMN markers of connectivity, with corresponding behavioral improvements. Voss and colleagues, for example, found that a 12-month aerobic exercise program among older adults enhanced ECN and DMN connectivity, with corresponding improvements in executive function ( 57 ). The DMN, in particular, has been extensively studied for its responsivity to exercise training ( 58 ), as well as being widely implicated in the pathogenesis of depression ( 59 , 60 ), particularly LLD ( 59 , 60 ). In addition, a growing body of work suggests that greater baseline evidence of disrupted connectivity is predictive of subsequent behavioral improvements in markers of cognitive control ( 55 , 56 ). Similar findings have been reported for mood improvements ( 61 ), with altered connectivity in DMN and ECN associating with poorer treatment outcomes and greater cognitive dysfunction among adults with depression ( 62 ).
Observed changes in connectivity are also likely attributable to enhancements of neurotransmitter systems, particularly neuromodulatory pathways (dopamine, norepinephrine, and (serotonin).
This assertion is supported by large amounts of indirect evidence suggesting that neurobehavioral improvements following exercise are largest in executive functions ( 17 , 18 ), which are preferentially impacted by dopaminergic disruption. In addition, parallel cognitive improvements are observed across heterogeneous populations with dysfunctional dopaminergic/norepinephrine functioning, including Parkinson’s disease ( 63 ), attention-deficit/hyperactivity disorder ( 64 , 65 ), and bipolar disorder ( 66 ), with exercise-related increases in dopamine production ( 67 ). Modulation of the serotonin system is also widely hypothesized to play an important mechanistic role in the effects of acute exercise training on mood-related changes ( 68 ), with at least one prior trial demonstrating that higher intensity of aerobic training increased plasma 5-HT levels, which associated with improved response inhibition ( 69 ). Taken together, these data suggest that enhanced production and synthesis of monoamines is a critical component of improved affect regulation and cognitive control, both of which enhance self-regulation.
In addition to direct modulation of cognitive and affective responses, exercise training may also facilitate learning of adaptive behavioral responses that improve mental health ( Figure 1 ), broadly formulated as self-regulatory capacities. While self-regulation is vast, it includes ER and cognitive control, which are transdiagnostic mechanisms of change. Consistent with the Science of Behavior Change initiative ( 70 ), these mechanisms should be evaluable and coherent at different levels of analysis (i.e., changes in behavioral mechanisms should correspond to neurobiological changes) and, by extension, could be mutually facilitative, such that changes in one affect the other. Although prior research has examined regulation of both emotion and affect, affect regulation has traditionally been defined as the modulation of emotions or emotional expression in the service of self-regulation. Affect regulation has also traditionally been more closely associated with executive functioning in comparison with ER.
There are few examples that integrate psychological and neurocognitive mechanisms in a single model. One possible exception is self-systems theory (SST) ( 71 – 73 ). According to SST, many psychological disorders result from cumulative or catastrophic failures of goal pursuits ( 72 ). SST has most widely been used in depression, where it is superior to conventional therapeutic approaches among depressed adults with self-regulatory deficits ( 71 ). However, a critical conceptual element of SST, which parallels mechanistic studies on PA and mental health, is its integration of both psychological function and neurobiological inefficiencies as contributing to potential self-regulatory failures within an individual. Differential impact of exercise on mental health could arise from either source or from a lack of effective synergy between the two. This concept may be critical in understanding for whom interventions work and under what conditions, and in tailoring treatments.
Specific behavioral mechanisms linking exercise interventions to mental health include self-regulatory skills specific to affect regulation ( 61 , 74 ) (e.g., tolerating and modulating arousal) and cognition ( 75 ) (e.g., exerting cognitive control over behavior, sustaining attention, and flexibly shifting attention and behavioral responses to match environmental demands) ( 76 ), which could influence mental health directly and through increased self-efficacy ( 77 ). Exercise may also potentiate reward salience through increased engagement in personally meaningful or rewarding activities and reward sensitization, or improved fitness (e.g., feeling more fit, improved body image). Behavioral mechanisms broadly correspond with neurological domains of changes, as summarized in Figure 3 .
Conceptual model of behavioral mechanisms by which exercise training improves mental health outcomes.
The impact of exercise on mood is one of the most widely studied mechanisms linking exercise to mental health, both through acutely enhancing mood and by improving ER during stressful life circumstances ( 78 ). Newer cognitive-behavioral therapies (CBTs), such as Acceptance and Commitment Therapy ( 77 ) and Dialectical Behavior Therapy, target difficulties in ER as a key mechanism of change ( 79 ). ER is a multidimensional construct that includes awareness and clarity of feelings, as well as acceptance of emotions and the ability to modulate emotional responses. A significant literature indicates that difficulties in ER are associated with mental health problems and that improvements in ER correspond with better mental health. A smaller literature demonstrates improvements in these processes prospectively predicting outcomes. Experiential avoidance and avoidant coping with unwanted thoughts and feelings (i.e., efforts to avoid or suppress thoughts/feelings) are particularly detrimental, contributing to the development and maintenance of anxiety disorders (including panic disorder), depression, substance abuse, and posttraumatic stress disorder (PTSD), among others. Related issues of hypervigilance, reactive or impulsive responding to internal cues, and difficulty labeling emotions (alexithymia or poor interoceptive awareness) are also implicated in psychiatric disorders, most notably PTSD, borderline personality disorder, and eating disorders.
Exercise may improve individuals’ ability to tolerate negative affect or high levels of arousal. For example, high-intensity exercise elicits autonomic arousal that mimics anxiety. During exercise, individuals experience these sensations in a nonthreatening context, in which aversive interoceptive cues are not only expected but may be indicative of effective engagement. This may form new associations with anxiety and increase capacity to tolerate interoceptive sensations while inhibiting avoidance/escape responses. Participants may also learn skills to modulate arousal, such as through paced breathing. Exercise training, particularly high intensity interval training and resistance training, also causes temporary discomfort in pursuit of a more long-term goal (e.g., fitness). The ability to allow short-term discomfort in favor of long-term gain is essential for impulse control. Repeated exercise training over the course of weeks and gradual intensity titration might be particularly effective in helping participants gain mastery over potentially distressing internal experiences. Exercise may therefore incorporate gradual exposure with response prevention in the context of training, similar to conventional psychotherapy paradigms using desensitization techniques through gradual exposure ( 80 – 82 ). Studies with various clinical populations have suggested that aerobic training reduces anxiety and anxiety sensitivity. Indeed, most of the brain regions that have enhanced activation and function following exercise training are well known for their importance in affective reactivity within the DMN pathways, particularly the ventromedial PFC and its regulation of reactivity within subcortical and insular brain regions ( 83 ). Decreased affect reactivity would be expected to decrease the need for unhealthy avoidance or suppression of emotional responses.
A separate line of research has examined changes in affective reactivity to provocative stimuli following exercise training in the setting of intentional weight loss. This work suggests that behavioral training exercise may diminish participant SN reactivity to salient food cues, particularly within the ventral striatum and insula ( 84 ). In a similar study using a crossover design ( 85 ), 60 min of exercise among habitual exercisers reduced activation in the putamen and peri-insular brain regions to high-energy food cues. Similarly, Cornier and colleagues ( 84 ) found that reductions in weight were associated with reduced insular activation among overweight/obese adults following a 6-month exercise trial. Taken together, this work suggests that exercise might decrease affective reactivity/saliency of food cues, increasing ability to control impulses or regulate eating behavior. Increased modulation of food responses may also have broader implications for cultivating impulse control and self-regulatory capacity, which holds importance for reduced substance use risk, behavioral impulsivity, and overall improvements in mental health functioning.
Exercise training programs often include behavior change strategies in the context of intervention delivery, particularly for home-based training paradigms. Behavior change strategies include behavioral self-regulatory skills such as goal setting, activity planning (including behavioral activation), adaptive problem solving, the provision of feedback, and self-monitoring ( 86 ), all of which overlap with key elements of traditional CBT. When these strategies are utilized in behavioral trials among individuals with mental health conditions, they likely play an active therapeutic role and may partially explain treatment improvements ( 87 ). As detailed below, effective behavioral engagement and self-monitoring are frequently impaired in individuals with depression and anxiety. Interventions cultivating these skill sets may therefore offer opportunities for experiential practice of clinically relevant skill domains in the service of exercise titration and maintenance.
Conventional exercise training programs teach participants to identify and implement goals that are specific, measurable, achievable, realistic, and timely (SMART goals), in order to optimize exercise participation and maintenance. Through the process of setting SMART goals, striving toward them, and evaluating iterative progress, participants cultivate realistic expectations for themselves and internalize a sense of behavioral control. Realistic goal setting and attainment also contribute to ER by increasing self-mastery, increasing agency, and establishing new, positive associations with self-concept. The process of self-monitoring (tracking behavior and its consequences) may also build a greater capacity to identify and repeat behaviors that are effective, as well as identifying maladaptive behavioral patterns.
Several mental health conditions, including depression and anxiety, are notable for impairments in cognitive flexibility and attentional control. Difficulties include poor set-shifting abilities (i.e., difficulty switching between tasks or altering behavior in response to feedback) ( 88 ), selective attention, and distractibility. Sustained attention and vigilance are also impaired across many mental health conditions, particularly in depression, where patients have difficulties sustaining engagement toward goal-directed targets over prolonged periods of time. Competing cognitive processes, such as rumination or excessive worry, may divert attention away from effective task performance and increase emotional suffering.
Impairments in cognitive control domains, including cognitive flexibility and executive function, have been repeatedly tied to behavioral treatment outcomes ( 89 – 91 ). Similarly, behavioral treatments improving cognitive flexibility and executive function also tend to favorably impact depression and anxiety outcomes ( 89 ). For example, cognitive flexibility is a putative treatment mechanism of mindfulness-based stress reduction, which has been shown to increase resting-state connectivity within ECN brain areas following training ( 92 ). As noted above, exercise training appears to have preferentially favorable effects on executive functions ( 76 ) and connectivity within ECN brain areas ( 57 ). Notably, poorer cognitive control is also a robust predictor of inadequate PA maintenance ( 28 , 93 ), suggesting that poorer cognitive control is likely to present barriers both for initial acquisition of self-regulatory skills for PA engagement and utilization of these skills for maintenance over time.
Several newer CBTs teach mindfulness to decrease engagement in unproductive mental activities and improve capacity to be in the present moment. Exercise training programs may increase the ability to direct and sustain attention to the present, particularly if exercises are sufficiently difficult. In this case, effective engagement in the activity requires full attention to the task and awareness of a narrowed set of stimuli (e.g., one’s breathing and ability to pace breathing). These behavioral mechanisms may change in tandem with neurobiological-mediated decreases in the saliency of some stimuli (described above) and potentiation of reward, as detailed below.
Individual self-regulatory behaviors are also important for mental health functioning through their overlapping influences on self-efficacy ( 73 ). Broadly defined, self-efficacy refers to an individual’s confidence in their ability to achieve specific, personally significant goals. Greater engagement in PA has been shown to increase exercise self-efficacy ( 73 ), associated with improved body image and physical quality of life, and increases the likelihood of sustained PA maintenance over time ( 94 ). In addition, many of the domains reviewed above align closely with key conceptual elements of improved self-efficacy, including monitoring of performance accomplishments, behavioral modeling, social persuasion, and adaptive interpretation of physiological states. Recent meta-analytic syntheses suggest that exercise interventions confer moderately large improvements in self-efficacy across adolescent and adult cohorts (ES = 0.59) ( 95 ). The total number of behavior change strategies demonstrates the strongest associations with improved PA, regardless of the specific strategy used ( 96 ).
A poverty of reinforcement or adaptive reward may lead to increased negative affect (e.g., depression) or the development of maladaptive behavior patterns to increase positive feelings (e.g., substance abuse). There is an extensive literature on increasing reinforcers/reward as a treatment mechanism of depression through behavioral activation ( 97 ). Newer CBTs, such as Acceptance and Commitment Therapy, link behavioral activation specifically to personal values, which may function to augment its reinforcement value or function as an establishing operation, and/or help sustain activity engagement. Behavioral activation often includes exercise or other forms of PA and may therefore both increase opportunities for positive reinforcement and cultivate realistic expectations regarding loss and reward, both of which may improve mental health. In addition, individual differences in reward sensitivity likely explain part of the observed heterogeneity in intermediate, positive consequences of PA (e.g., improved mood or fitness), which have been associated with the self-reinforcing nature of habitual PA and maintenance ( 74 ).
Dysfunctional reward sensitivity is a core feature increasing the risk of depression and serves as a key barrier to implementation of many therapeutic interventions. Exercise training has been postulated to improve reward sensitivity by augmenting dopaminergic function. Focusing on goal-directed behaviors has been shown to enhance top-down activation within the ventromedial PFC and ventral striatum, as well as downregulating insular and amygdala activation during stressful activities ( 98 ). Individuals engaging in habitual PA demonstrate differential activation of the ventral striatum, a critical dopamine hub, compared to their sedentary counterparts following acute exercise training ( 99 ). Individuals accustomed to habitual PA also show improved reward system functioning compared to sedentary counterparts, a relationship that does not appear to differ based on physical fitness ( 100 ).
Clearly specifying both neurological and behavioral mechanisms that link exercise to mental health and how they might interact synergistically to produce outcomes may have implications for the design of exercise programs to potentiate training engagement and optimize outcomes for individuals or groups of individuals. Pre-existing neurobiological differences might explain the extent to which exercise interventions are effectively engaged and/or suggest indirect mechanisms of benefit in the context of exercise training. Repeated measurement and network analyses may be able to help disentangle the associations among elements that are probably mutually facilitative.
As reviewed above, both neurobiological markers of neuroplasticity and behavioral markers of self-regulatory function hold relevance in the development of future exercise training paradigms. Future studies should integrate phenotypic markers of neuroplasticity into intervention development in order to optimize intervention engagement. For example, individuals with blunted reward sensitivity may have difficulty with initial exercise engagement and therefore be less likely to adequately engage with or complete supervised training programs. These individuals may benefit from more gradual titration of activity, motivational priming prior to training sessions, or enhancement of reward reinforcement cues using external sources. Similarly, individuals with evidence of cognitive inflexibility and/or executive dysfunction may have difficulty with exercise maintenance and could benefit from receiving either greater external regulatory support (e.g., structured classes or exercise with a spouse) or additional self-management training to increase the likelihood of continued PA for optimal ER.
Future studies should also systematically assess and quantify individual differences in self-regulatory skills across participants, both as a baseline predictor of treatment engagement and across time as a mechanism of treatment improvements. Specifying individual differences in self-regulatory skills at baseline might also allow for effective treatment matching (matching individuals to exercise programs that they are more likely to be successful with or to programs that are more likely to address skill deficits and improve overall health and well-being) or tailoring of existing interventions to optimize outcomes. For example, individuals with difficulty regulating affect may also tend to avoid emotional or interoceptive discomfort, and they may experience increased sensitivity to arousal due to either distressing past experiences or inaccurate beliefs that arousal is dangerous. Irrespective of its precise origin, this behavioral tendency would suggest the need for differential titration of activity, greater usage of distraction techniques, or self-monitoring for titration based on external biometric sources (e.g., heart rate) that are not overly dependent on self-referential attention to interoceptive cues. These participants could also be trained to gain mastery by resisting urges to avoid or escape aversive cues or to use strategies to modulate arousal such that it can be sustained during a window of tolerance, which may be gradually expanded over time.
In addition, future RCTs may benefit from the use of optimization designs to determine the relative importance of priming neuroplasticity in order to achieve better mental health outcomes. RCTs utilizing sequential randomization to treat depression, for example, could re-randomize participants contingent upon connectivity or executive functioning changes, suggesting enhanced neuroplasticity as an intermediate marker of treatment responsivity. Similarly, trials examining exercise maintenance could benefit from provision of external support strategies among individuals with poorer self-regulatory capacity, including integration of social support or greater ease of access to exercise training equipment. Because these individuals will be less likely to self-initiate behavioral modifications or flexibly adapt their behavioral responses for exercise maintenance, additional environmental support is critical for outcomes.
In conclusion, aerobic and resistance exercise training hold promise in the treatment and management of mental health conditions, particularly depression and anxiety. Emerging evidence suggests that changes in underlying neuroplasticity may be an important individual difference explaining heterogeneous treatment benefits. In addition, underlying individual differences in neuroplasticity, either at baseline or in intervention-related changes, likely have significant implications for individuals developing and sustaining behavioral self-regulatory skills essential for mental health. These factors likely work in synergy, creating a “virtuous cycle” to predict long-term effects of exercise on mental health. By clearly specifying both neurobiological and behavioral mechanisms linking exercise to improved mental health, it may be possible to optimize treatment effects and personalize training approaches for maximal benefit.
LLD: late-life depression
SN: salience network
ECN: executive control network
DMN: default mode network
ER: emotion regulation
Dr. Smith thanks Erica Shirts, Jeanne Schwartz, Bryan Feger, and Timothy Strauman for their thoughtful input during the conceptual formulation of this manuscript. This research was supported by funding from the National Institute of Health, NHLBI Grant R01HL130237.
DISCLOSURE STATEMENT
The authors are not aware of any affiliations, memberships, funding, or financial holdings that might be perceived as affecting the objectivity of this review.
COMMENTS
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