Psychiatry Research 145 (2006) 79 83
www.elsevier.com/locate/psychres
Hypothesis
Transient hypofrontality as a mechanism for the psychological
effects of exercise
N
Arne Dietrich
Department of Social and Behavioral Sciences, American University of Beirut, Beirut, Lebanon
Received 11 September 2003; received in revised form 24 January 2004; accepted 10 July 2005
Abstract
Although exercise is known to promote mental health, a satisfactory understanding of the mechanism underlying this
phenomenon has not yet been achieved. A new mechanism is proposed that is based on established concepts in cognitive
psychology and the neurosciences as well as recent empirical work on the functional neuroanatomy of higher mental processes.
Building on the fundamental principle that processing in the brain is competitive and the fact that the brain has finite metabolic
resources, the transient hypofrontality hypothesis suggests that during exercise the extensive neural activation required to run motor
patterns, assimilate sensory inputs, and coordinate autonomic regulation results in a concomitant transient decrease of neural
activity in brain structures, such as the prefrontal cortex, that are not pertinent to performing the exercise. An exercise-induced state
of frontal hypofunction can provide a coherent account of the influences of exercise on emotion and cognition. The new hypothesis
is proposed primarily on the strength of its heuristic value, as it suggests several new avenues of research.
© 2006 Elsevier Ireland Ltd. All rights reserved.
Keywords: Anxiety; Cognition; Consciousness; Depression; Emotion; Prefrontal cortex; Stress
1. Introduction mechanistic explanation is still lacking. Previous research
has concentrated heavily on alterations in neurotransmit-
Exercise is beneficial to mood and cognition (e.g., ter mechanisms such as norepinephrine (Dishman, 1997),
Colcombe and Kramer, 2003; Scully et al., 1998; Tom- endorphins (Hoffman, 1997), serotonin (Chaouloff,
porowski, 2003). Extensive evidence shows that in the 1997), and most recently endocannabinoids (Sparling et
moderate, aerobic range, exercise reduces stress, de- al., 2003; Dietrich and McDaniel, 2004). Bearing on this
creases anxiety, and alleviates depression (Salmon, 2001). long-standing gap in the medical knowledge base, it will
Despite decades of research attempting to explicate a be shown that established concepts in cognitive psychol-
neurochemical basis for these phenomena, a sound ogy and the neurosciences, coupled with recent findings
intimating prefrontal cortex pathology in anxiety dis-
orders and depression, can be synthesized to formulate a
new hypothesis. This surprisingly simple hypothesis,
N
Department of Social and Behavioral Sciences American Univer-
transient hypofrontality , is based on functional neu-
sity of Beirut, P.O. Box 11-0236, Riad El-Solh/Beirut 1107-2020,
roanatomy and should be regarded as complementary to
Lebanon. Tel.: +961 1 350000x4365.
E-mail address: arne.dietrich@aub.edu.lb. explanations focusing on neurotransmitter changes.
0165-1781/$ - see front matter © 2006 Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.psychres.2005.07.033
80 A. Dietrich / Psychiatry Research 145 (2006) 79 83
Importantly, this new theoretical framework yields a study in which rats ran for 30 min on a treadmill at 85%
number of eminently testable hypotheses. of maximum O2 uptake, found highly significant
increases in LCGU in all brain structures except in
2. Exercise-induced transient hypofrontality prefrontal cortex, frontal cortex, cingulum, CA3, medial
nucleus of the amygdala, lateral septal area, nucleus
Converging evidence from a number of techniques accumbens, a few hypothalamic nuclei, median raphe
(133Xe washout, radioactive microsphere, and autoradi- nucleus, interpeduncular nucleus, nucleus of the solitary
ography as well as EEG, SPECT, and PET) has shown tract, and inferior olive. Taken together, these neural
that exercise is associated with profound regional regions represent but a small percentage of total brain
changes in motor, sensory, and autonomic regions of mass, confirming that physical exercise requires mas-
the brain. Marked increases in activation occur in neural sive neural activation in a large number of neural
structures responsible for generating the motor patterns structures across the entire brain. It follows that
that sustain the physical activity. In particular, the prolonged, aerobic exercise would require the sustained
primary motor cortex, secondary motor cortices, basal activation of such a large amount of neural tissue.
ganglia, cerebellum, various midbrain and brainstem Despite such marked regional increases, global blood
nuclei, motor pathways, and several thalamic nuclei are flow to the brain during exercise, as well as global
involved. Exercise also activates structures involved in cerebral metabolism and oxygen uptake, remains
sensory, autonomic, and memory function, particularly constant (Ide and Secher, 2000; Sokoloff, 1992). During
primary and secondary sensory cortices, sensory path- exercise, the percentage of total cardiac output to the
ways, brainstem nuclei, hypothalamus, and the sensory brain is drastically reduced as blood is shunted from
thalamus. Cerebral blood flow (CBF) and local cerebral numerous areas, including the brain, to the muscles
glucose utilization (LCGU) and metabolism, both sustaining the workload. At maximal exercise, the brain
indexes of the functional activity of neurons, have receives approximately four times less volume per heart-
confirmed this pattern of neural activity in exercising beat, as compared with the resting state. This reduction is
non-human animals (e.g., Gross et al., 1980; Holschnei- precisely offset by the overall increase in cardiac output
der et al., 2003; Sokoloff, 1992; Vissing et al., 1996). In during exercise (Astrand and Rodahl, 1986). The result
the most comprehensive study to date, Vissing et al. of this interaction is a constant and steady perfusion rate.
(1996) concluded that marked exercise-induced Thus, contrary to popular conception, there is no
increases in LCGU were found in cerebral gray matter evidence to suggest that the brain is the recipient of
structures involved in motor, sensory, and autonomic additional metabolic resources during exercise (Dietrich,
function as well as in white matter structures in the 2003).
cerebellum and corpus callosum (p. 731). As a consequence of the brain s finite resources,
Physiological data on human brain activity during humans possess a limited information-processing ca-
exercise are remarkably sparse but consolidate, not pacity. This is not only true at the bottleneck of
surprisingly, the data in the animal literature. In the only consciousness (Broadbent, 1958), where our limited in-
PET study published to date, increased brain activation formation-processing capacity is a well-established
was recorded in the primary sensory cortex, primary concept that forms one of the cornerstones of cognitive
motor cortex, supplementary motor cortex as well as the science, but there also exists a total cap on all neural
anterior part of the cerebellum (p. 66) in response to activity, including unconscious, parallel information
cycling (Christensen et al., 2000), while the only processing. In other words, because the brain cannot
published single photon emission computed tomography maintain activation in all neural structures at once, the
study found increases in regional CBF in the supple- activation of a given structure must come at the expense
mentary motor area, medial primary sensorimotor area, of others. Such need-based shifts of resources have been
striatum, visual cortex, and cerebellar vermis during observed at a smaller scale in response to treadmill
walking (Fukuyama et al., 1997). walking. Using a rat model, Holschneider et al. (2003)
There appears to be a pervasive tendency to grossly reported that the significant decreases in CBF-TR noted
underestimate the amount of brain tissue that must be in primary somatosensory cortex mapping the barrel
activated for the supposedly simple act of moving. It field, jaw, and oral region suggests a redistribution of
should be noted that a large part of the brain is devoted perfusion away from these areas during the treadmill
to basic sensory/perceptual processes, autonomic regu- task (p. 929). Naturally, such costs and benefits
lation, and motor output and must be engaged during associated with efficient information processing are a
physical activity. For instance, Vissing et al. (1996), ina direct consequence of the principles of evolution
A. Dietrich / Psychiatry Research 145 (2006) 79 83 81
(Edelman, 1993). Indeed, the hypothesis is consistent support for the hypothesis that exercise decreases neural
with the more general proposal of competitive interac- activity in the prefrontal cortex. As cited above, Vissing
tions in a variety of brain systems (Desimone and et al. (1996) found highly significant increases in LCGU
Duncan, 1995; Miller and Cohen, 2001). Thus, in in all but a few brain structures, including the prefrontal
addition to competing for access to consciousness, cortex. This pattern of activity is so striking that extended
brain structures are subjected to an overall information- aerobic running could be regarded as a state of
processing limit due to finite metabolic resources. generalized brain activation with the specific exclusion
Evidence that sensory motor integration tasks in- of the executive system (as the other structures in this
volving large-scale bodily movement, such as physical study do not constitute a large volume of neural tissue).
exercise, require massive and sustained neural activation Additional evidence for the hypothesis comes from a
of sensory, motor, and autonomic systems (Vissing et al., human study that correlated the rating of perceived
1996), coupled with the fact that the brain operates on a exertion (RPE) with EEG activity (Nybo and Nielsen,
fixed amount of metabolic resources (Ide and Secher, 2001). Recording from three placements (frontal,
2000), suggests that exercise must place a severe strain central, and occipital cortex) during submaximal
on the brain s limited information-processing capacity. exercise, Nybo and Nielsen found that altered EEG
This should result in a concomitant transient decrease in activity was observed in all electrode positions, and
neural activity in structures that are not directly essential stepwise forward-regression analysis identified core
to the maintenance of the exercise (Dietrich, 2003). Put temperature and a frequency index of the EEG over
another way, the brain downregulates neural structures the frontal cortex as best indicators of RPE (p. 2017).
performing functions that an exercising individual can This finding suggests that exercise is not only associated
afford to disengage (Dietrich, 2004). This notion is a with decreases in frontal activity but also that the degree
consequence of the fundamental principle that proces- of physical effort might be correlated with the severity
sing in the brain is competitive (Miller and Cohen, of frontal deactivation.
2001). Depending on the type of sport, the transient Despite this converging evidence, it is not clear how
hypofrontality hypothesis proposes that these areas are, these largely physiological data that support a state of
first and foremost, the higher cognitive centers of the transient hypofrontality correlate with psychological
frontal lobe, and, to a lesser extent, emotional structures function during exercise, particularly mental processes
such as the amygdala. subserved by the prefrontal cortex such as working
The transient hypofrontality hypothesis is supported memory, sustained and directed attention, and complex
by several lines of evidence. Numerous EEG studies have social emotions.
consistently shown that exercise is associated with alpha
and theta enhancement, particularly in the frontal cortex 3. Implications for mental health
(Boutcher and Landers, 1988; Kamp and Troost, 1978;
Kubitz and Pothakos, 1997; Nybo and Nielsen, 2001; Because neuroimaging studies of individuals with
Petruzzello and Landers, 1994; Pineda and Adkisson, anxiety disorders and depression show evidence of
1961; Youngstedt et al., 1993). An increase in alpha frontal lobe dysfunction, the concept of exercise-
activity is a putative indicator of decreased brain induced transient hypofrontality suggests a new neural
activation (Kubitz and Pothakos, 1997; Petruzzello and mechanism by which exercise might be beneficial to
Landers, 1994). For instance, Kubitz and Pothakos (1997) mental health. Briefly, in obsessive compulsive disor-
concluded that exercise reliably increases EEG alpha der (OCD), for instance, the ventromedial prefrontal
activity (p. 299), while Petruzzello and Landers (1994) cortex (VMPFC), which has been implicated in complex
stated that there was a significant decrease in right frontal emotions, exhibits widespread hypermetabolism
activation during the post-exercise period (p. 1033). (Baxter, 1990), while individuals with other anxiety
Single cell recording in exercising cats has also disorders, such as posttraumatic stress disorder or
provided support for decreased activation in prefrontal phobia, show hyperactivity in the amygdala (LeDoux,
regions. In recordings from 63 neurons in the prefrontal 1996). Given the analytical, emotional and attentional
cortex, units associated with the control of movement capacities of the prefrontal cortex, the excessive activity
showed increased activity during locomotion, while is thought to generate a state of hyper-vigilance and
other prefrontal units decreased their discharge (Criado hyper-awareness leading to anxiety. PET studies reveal a
et al., 1997). similar picture for depression, which is also marked by
Studies on CBF and metabolism (e.g., Gross et al., hyperactivity in the VMPFC and the amygdala (May-
1980; Vissing et al., 1996) have provided the strongest berg, 1997). Conversely, the dorsolateral prefrontal
82 A. Dietrich / Psychiatry Research 145 (2006) 79 83
cortex (DLPFC), which is associated with higher This temporal resolution is the very basis of interpreting
cognitive functions, shows less than normal activity in functional neuroimaging studies. In an EEG study using
depression, depriving the individual of the higher exercising cats, Ángyán and Czopf (1998) also reported
cognitive abilities that might help mitigate the negative that during rest, the pre-running brain activity gradually
mood. Treatment with selective serotonin reuptake reappeared (p. 267). This indicates that a delay of even
inhibitors (SSRIs) results in a normalization of the mal- a few minutes would be sufficient to normalize any
functioning of this complex prefrontal circuitry (May- exercise-induced changes in neural activity and studies
berg et al., 1995), pointing to an abnormal interaction using a delay cannot be used to interpret congition
between the VMPFC and the DLPFC rather than global during exercise. Thus, the transient hypofrontality
prefrontal dysfunction (Starkstein and Robinson, 1999). hypothesis should be regarded as a limited domain
Interestingly, healthy subjects asked to think sad thoughts hypothesis that emphasizes immediate effects of exer-
show a similar pattern of activity (Damasio et al., 2000). cise on psychological function. Undoubtedly, consider-
Considering the similarities in brain activation, it is not ably more research is needed to clarify the effects of
surprising that OCD patients frequently develop comor- acute exercise on brain function and how this might
bid major depression, and that the treatment of choice for affect mental ability in the long term.
both disorders is SSRIs (Starkstein and Robinson, 1999).
The transient hypofrontality hypothesis proposes that 4. Conclusions
exercise exerts some of its anxiolytic and antidepressant
effects by inhibiting the excessive neural activity in Supportive evidence from exercise science, psychol-
VMPFC regions, and thus reducing the relative imbal- ogy, and neuroscience was synthesized to develop a new
ance between VMPFC and DLPFC activity. In other mechanistic explanation for the anxiolytic, antidepres-
words, physical exercise involving large-scale bodily sant, and cognitive effects accompanying acute exercise.
motion requires massive neural activity and thus places a The transient hypofrontality hypothesis is based on
strain on the brain s finite neural resources, making it neuroanatomical, physiological, and theoretical consid-
impossible to sustain excessive neural activity in erations and has several advantages over other ap-
structures, such as the prefrontal cortex and the proaches. First, a state of diminished activity in prefrontal
amygdala, that are not needed at the time. As the brain regions can account for a wide variety of well-
must run on safe mode the very structures that appear to documented cognitive and emotional changes associated
compute the information, engendering stress, anxiety, with exercise. Second, unlike other theories, it can
and negative thinking, we experience relief from life s provide a coherent psychological explanation of the EEG
worries due to phenomenological subtraction. data in humans and the single cell recording in animals, as
In the cognitive domain, the transient hypofrontality well as the blood flow and metabolism data from both
hypothesis predicts that higher cognitive processes non-humans and humans. Third, it is presently the only
supported by the prefrontal cortex are selectively im- theoretical framework that accommodates current data on
paired during exercise. Using putative neuropsycholog- the neuroanatomy of anxiety disorders and depression.
ical measures that are sensitive to prefrontal impairment Most importantly, however, the hypothesis opens
such as the Wisconsin Card Sorting Task, the Paced unexpected avenues of research and provides a coherent
Auditory Serial Addition Task, or the Stroop Test, we account of the data on the influences of acute exercise
predicted that an individual s ability to perform tasks on mental processes and psychological well-being.
known to heavily recruit prefrontal circuits should be Although considerable evidence points to prefrontal
selectively impaired during endurance exercise, while downregulation during exercise, direct measures of
tasks requiring little prefrontal activation should be transient hypofrontality are necessary to substantiate the
unaffected. Our results showed that this is indeed the hypothesis.
case (Dietrich and Sparling, 2004), indicating that a non-
cognitive task, such as running on a treadmill, can
References
constrain recourses available for cognition. These
results do not contradict other findings suggesting cog- Ángyán, L., Czopf, J., 1998. Exercise-induced slow waves in the EEG
of cats. Physiology and Behavior 64, 268 272.
nitive enhancement following exercise (Colcombe and
Astrand, P., Rodahl, K., 1986. Textbook of Work Physiology, 3rd ed.
Kramer, 2003). To illustrate, neuroimaging studies show
McGraw-Hill, New York.
that the pattern of neural activation associated with a
Baxter, L.R., 1990. Brain imaging as a tool in establishing a theory of
particular task is unique to that task and returns to
brain pathology in obsessive compulsive disorder. Journal of
baseline levels shortly after the cessation of that task. Clinical Psychiatry 5, 22 25.
A. Dietrich / Psychiatry Research 145 (2006) 79 83 83
Boutcher, S.J., Landers, D.M., 1988. The effects of vigorous exercise Ide, K., Secher, N.H., 2000. Cerebral blood flow and metabolism
on anxiety, heart rate, and alpha enhancement of runners and during exercise. Progress in Neurobiology 61, 397 414.
nonrunners. Psychophysiology 25, 696 702. Kamp, A., Troost, J., 1978. EEG signs of cerebrovascular disorder,
Broadbent, D.A., 1958. Perception and Communication. Pergamon, using physical exercise as a provocative method. Electroenceph-
New York. alography and Clinical Neurophysiology 45, 295 298.
Chaouloff, F., 1997. The serotonin hypothesis. In: Morgan, W.P. (Ed.), Kubitz, K.A., Pothakos, K., 1997. Does aerobic exercise decrease
Physical Activity and Mental Health. Taylor & Francis, Washing- brain activation? Journal of Sport and Exercise Psychology 19,
ton, DC, pp. 179 198. 291 301.
Christensen, L.O., Johannsen, P., Sinkjaer, N., Peterson, N., Pyndt, H.S., LeDoux, J., 1996. The Emotional Brain. Touchstone, New York.
Nielsen, J.B., 2000. Cerebral activation during bicycle movements in Mayberg, H.S., 1997. Limbic-cortical dysregulation: a proposed
man. Experimental Brain Research 135, 66 72. model of depression. Journal of Neuropsychiatry and Clinical
Colcombe, S., Kramer, A.F., 2003. Fitness effects on the cognitive Neuroscience 9, 471 481.
function of older adults: a meta-analytical study. Psychological Mayberg, H.S., Mahurin, R.K., Brannon, K.S., 1995. Parkinson s
Science 14, 125 130. depression: discrimination of mood-sensitive and mood-insensi-
Criado, J.M., de la Fuente, A., Heredia, M., Riolobos, A.S., Yajeya, J., tive cognitive deficits using fluoxetine and FDG PET. Neurology
1997. Electrophysiological study of prefrontal neurons of cats 45, A166.
during a motor task. European Journal of Physiology 434, 91 96. Miller, E.K., Cohen, J.D., 2001. An integrative theory of prefrontal
Damasio, A.R., Graboweski, T.J., Bechera, A., Damasio, H., Ponto, L.L.B., cortex function. Annual Review of Neuroscience 24, 167 202.
Parvizi, J., Hichwa, R.D., 2000. Subcortical and cortical brain activity Nybo, L., Nielsen, B., 2001. Perceived exertion is associated with an
during the feeling of self-generated emotions. Nature Neuroscience 3, altered brain activity during exercise with progressive hyperther-
1049 1056. mia. Journal of Applied Physiology 91, 2017 2023.
Desimone, R., Duncan, J., 1995. Neural mechanisms of selective Petruzzello, A., Landers, D.M., 1994. State anxiety reduction and
visual attention. Annual Review of Neuroscience 18, 193 222. exercise: does hemispheric activation reflect such changes?
Dietrich, A., 2003. Functional neuroanatomy of altered states of Medicine and Science in Sports and Exercise 26, 1028 1035.
consciousness: the transient hypofrontality hypothesis. Conscious- Pineda, A., Adkisson, M.A., 1961. Electroencephalographic studies in
ness and Cognition 12, 231 256. physical fatigue. Texas Reports on Biology and Medicine 19,
Dietrich, A., 2004. Neurocognitive mechanisms underlying the 332 342.
experience of flow. Consciousness and Cognition 13, 746 761. Salmon, P., 2001. Effects of physical exercise on anxiety, depression,
Dietrich, A., McDaniel, W.F., 2004. Cannabinoids and exercise. and sensitivity to stress: a unifying theory. Clinical Psychology
British Journal of Sports Medicine 38, 50 57. Review 21, 33 61.
Dietrich, A., Sparling, P.B., 2004. Endurance exercise selectively Scully, D., Kremer, J., Meade, M.M., Graham, R., Dudgeon, K., 1998.
impairs prefrontal-dependent cognition. Brain and Cognition 55, Physical exercise and psychological well being: a critical review.
516 524. British Journal of Sports Medicine 32, 111 120.
Dishman, R.K., 1997. The norepinephrine hypothesis. In: Morgan, W. Sokoloff, L., 1992. The brain as a chemical machine. Progress in Brain
P. (Ed.), Physical Activity and Mental Health. Taylor & Francis, Research 94, 19 33.
Washington, DC, pp. 199 212. Sparling, P.B., Giuffrida, A., Piomelli, D., Rosskopf, L., Dietrich, A.,
Edelman, G.M., 1993. Neural Darwinism: selection and reentrant 2003. Exercise activates the endocannabinoid system. NeuroRe-
signaling in higher brain function. Neuron 10, 115 125. port 14, 2209 2211.
Fukuyama, H., Ouchi, Y., Matsuzaki, S., Nagahama, Y., Yamauchi, H., Starkstein, S.E., Robinson, R.G., 1999. Depression and frontal lobe
Ogawa, M., Kimura, J., Shibasaki, H., 1997. Brain functional disorders. In: Miller, B.L., Cummings, J.L. (Eds.), The Human
activity during gait in normal subjects: a SPECT study. Frontal Lobes: Functions and Disorders. The Guilford Press, New
Neuroscience Letters 228, 183 186. York, pp. 247 260.
Gross, P.M., Marcus, M.L., Heistad, D.D., 1980. Regional distribution Tomporowski, P.D., 2003. Effects of acute bouts of exercise on
of cerebral blood flow during exercise in dogs. Journal of Applied cognition. Acta Psychologica 112, 297 324.
Physiology 48, 213 217. Vissing, J., Anderson, M., Diemer, N.H., 1996. Exercise-induced
Hoffman, P., 1997. The endorphin hypothesis. In: Morgan, W.P. (Ed.), changes in local cerebral glucose utilization in the rat. Journal of
Physical Activity and Mental Health. Taylor & Francis, Washing- Cerebral Blood Flow and Metabolism 16, 729 736.
ton, DC, pp. 161 177. Youngstedt, S., Dishman, R.K., Cureton, K., Peacock, L., 1993. Does
Holschneider, D.P., Maarek, J.-M.I., Yang, J., Harimoto, J., Scremin, O.U., body temperature mediate anxiolytic effects of acute exercise?
2003. Functional brainmappinginfreelymovingratsduringtreadmill Journal of Applied Physiology 74, 825 831.
walking. Journal of Cerebral Blood Flow and Metabolism 23,
925 932.
Wyszukiwarka
Podobne podstrony:
[Pargament & Mahoney] Sacred matters Sanctification as a vital topic for the psychology of religionPopper Two Autonomous Axiom Systems for the Calculus of ProbabilitiesBattle For The Planet Of The Ap(business ebook) The Psychology of Color and Internet Marketing[Emmons & Paloutzian] The psychology of religionAntidepressants for the treatment of depression in children and adolescentsEvaluation of HS SPME for the analysis of volatile carbonyl(Trading) Paul Counsel Towards An Understanding Of The Psychology Of Risk And Succes2 11 The Psychology of the selves&the Awareness Ego Processabba two for the price of oneABBA Two for the Price of oneBroad; Arguments for the Existence of God(1)INTERACTION OF IONIC LIQUIDS WITH POLYSACCHARIDES 5 SOLVENTS AND REACTION MEDIA FOR THE MODIFICATIOwięcej podobnych podstron