Research reportAcute aerobic exercise enhances attentional modulation of somatosensory event-related potentials during a tactile discrimination task
Introduction
Selective attention is commonly referred to as a higher-order executive process that requires conscious allocation of cognitive resources toward relevant information in the presence of environmental distracters. Attention-related neuroimaging studies have shown that attending to task-relevant sensory information can activate a widespread neural network consisting of cortical and subcortical structures [1], [2], as well as enhance neuronal responses in modality-specific sensory cortices [3], [4], [5]. It is thought that attentional control is mediated by the prefrontal cortex (PFC) which operates as an inhibitory-control filtering mechanism, suppressing irrelevant sensory information so that relevant sensory signals can be amplified and passed on for further processing in modality-specific brain regions [6], [7]. Indeed, neuroimaging findings in healthy adults have shown attention-related neuronal enhancement of task-relevant tactile stimuli in frontal and modality-specific somatosensory regions [8], [9], while studies in patients with focal frontal lobe lesions have found that PFC damage produces disinhibition of distractor stimuli during a range of sensorimotor and cognitive processes [10]. Furthermore, a recent imaging study in healthy young adults showed that transient disruption to neuronal activity in dorsolateral PFC via continuous theta burst stimulation (cTBS), produced disinhibition of task-irrelevant stimuli at early and later stages of somatosensory processing during a tactile discrimination task [11]. A follow-up study in PFC patients using the same tactile discrimination task showed similar aberrations in the neuronal profile of some of the same early and late somatosensory ERPs found following cTBS to the dorsolateral PFC [12]. Collectively, these studies support the notion that the PFC has a critical role in mediating attentional control over incoming sensory information by suppressing irrelevant sensory signals so that attended task-relevant information may be amplified in modality-specific sensory regions.
Notably, a growing body of evidence suggests that a single bout of acute aerobic exercise improves cognitive performance and produces neurophysiological changes, particularly in frontal lobe regions, during tasks requiring selective attention [13], [14], [15]. Moreover, studies examining acute exercise-induced effects on cognition report that the greatest increases in neuronal activity are found in frontal regions following moderate bouts of aerobic exercise when tasks requiring higher-order attentional control are utilized [16], [17], [18], [19]. These exercise effects on attentional processing support the inverted U-shape arousal hypothesis first proposed by Yerkes and Dodson (1908), which states that as arousal states increase with physical exertion, cognitive performance improves to an optimal point after which further increases in physical exertion cause decreased arousal levels resulting in decrements in performance [20]. However, the majority of human neuroimaging studies have employed psychological tasks tailored to examine the effects of exercise on PFC function (i.e. the Erikson Flanker, Stroop, or go/nogo tasks). As a result, it remains unclear if acute aerobic exercise modulates cortical activity downstream from the PFC in modality-specific sensory regions. Investigating the effects of aerobic exercise on frontoparietal interactions is an important avenue of the exercise and cognition research to pursue since the circuitry of the PFC is complex with reciprocal corticocortical and thalamocortical connections involved in modulating modality-specific sensory regions via attentional mechanisms. Determining whether acute bouts of aerobic exercise can improve attentional regulation over modality-specific sensory cortices provides an additional perspective regarding how exercise may transiently improve cognitive function perhaps via more efficient modulation between corticocortical networks. Notably, an EEG study performed in soccer athletes and non-athletes using a lower limb somatosensory stimulation oddball task showed that the athletic group demonstrated increased P300 amplitudes and decreased latencies over central-parietal electrode sites compared to the non-athletic group [21]. These findings imply that long-term physical activity that requires selective attention and skilled motor responses may induce plastic changes in somatosensory processing during the execution of goal-oriented behaviors [21]. However, no exercise intervention was implemented in this study, thus a causal link between the effects of exercise on somatosensory processing cannot be determined.
The purpose of the present study was to use EEG and a well-established tactile discrimination task to examine whether an acute bout of moderate intensity aerobic exercise, would enhance attention-based modulation of somatosensory ERPs generated at early and later stages of somatosensory processing in healthy young adults. Based on the findings of Bolton and Staines [11], our first hypothesis was that early and later somatosensory ERPs would be modulated by attentional relevance. Specifically, we hypothesized that an acute bout of moderate intensity aerobic exercise preceding performance of a tactile discrimination task would result in more efficient sensory-gating of irrelevant/non-attended and enhancement of relevant/attended sensory information. Therefore, improvements in sensory-gating would be observed as increased neural suppression of task-irrelevant stimuli and enhancement of relevant sensory information post-relative to pre-exercise.
Section snippets
Participants
EEG was collected from 16 healthy participants (aged 21–28, 6 males). One participant was excluded due to the absence of clearly defined somatosensory event-related potentials of interest (i.e. P50, P100, N140, LLP components). The final sample consisted of 9 females and 6 males (mean age = 25.2 years). Participants were self-reported right-handed individuals with no medical history of any major neurological illness, and no heart or blood pressure conditions that could be exacerbated with aerobic
Early ERP components: P50 & P100
Fig. 2 shows waveforms at electrode sites contralateral to vibrotactile stimulation (i.e. FC4, CP4, and P4) with the components of interest specified (i.e. the P50, P100, N140, and LLP). Results for the P50 amplitude revealed no main effects or significant interaction at any of the electrode sites analyzed. Results for the P100 component showed a main effect of attention whereby P100 amplitudes were enhanced by task-relevant stimuli (i.e. Attend Index) compared to task-irrelevant stimuli (i.e.
Discussion
Evidence suggests that acute aerobic exercise selectively up-regulates excitability in frontal lobe regions, thereby promoting greater top-down attentional control during executive functioning tasks [13], [14], [15]. However, the effects of acute exercise in cortical areas downstream from the PFC in modality-specific cortices are not well understood. This study examined how an acute bout of moderate intensity aerobic exercise modulated neuronal activity in somatosensory cortices using a tactile
Conclusion
Our results suggest that an acute bout of moderate intensity aerobic exercise facilitated selective attentional processing of somatosensory information by improving: i) the efficiency of involuntary attentional shifts toward task-irrelevant environmental distracters over modality-specific somatosensory regions, and ii) attentional control of somatosensory input at later stages of sensory processing over frontoparietal regions. These findings imply that an acute bout of moderate intensity
Acknowledgements
This work was supported by funding to WRS from the Natural Sciences and Engineering Research Council of Canada (NSERC), the Canada Research Chairs program, the Canada Foundation for Innovation and the Ontario Research Fund. CP was supported by graduate scholarship funds from the Ontario Graduate Scholarship (OGS) program.
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