Identification of higher brain centres that may encode the cardiorespiratory response to exercise in humans (original) (raw)

Identifying cardiorespiratory neurocircuitry involved in central command during exercise in humans

The Journal of Physiology, 2006

For almost one hundred years, the exact role of human brain structures controlling the cardiorespiratory response to exercise ('central command') has been sought. Animal experiments and functional imaging studies have provided clues, but the underlying electrophysiological activity of proposed relevant neural sites in humans has never been measured. In this study, local field potentials were directly recorded in a number of 'deep' brain nuclei during an exercise task designed to dissociate the exercise from peripheral feedback mechanisms. Several patient groups had electrodes implanted sterotaxically for the treatment of movement disorder or chronic pain. Fast Fourier transform analysis was applied to the neurograms to identify the power of fundamental spectral frequencies. Anticipation of exercise resulted in increases in heart rate, blood pressure and ventilation. The greatest neural changes were found in the periaqueductal grey area (PAG) where anticipation of exercise was accompanied by an increase of 43% in the power of the 12-25 Hz frequency band (P = 0.007). Exercise increased the activity by 87% compared to rest (P = 0.006). Changes were also seen in the 60-90 Hz band when anticipation or exercise increased power by 32% (P = 0.006) and 109% (P < 0.001), respectively. In the subthalamic nucleus there was a reduction in the power of the beta frequency during both anticipation (7.6 ± 0.68% P = 0.001) and exercise (17.3 ± 0.96% P < 0.001), whereas an increase was seen with exercise only at higher frequencies (93 ± 1.8% P = 0.007). No significant changes were seen in the globus pallidus during anticipation of exercise. We provide direct electrophysiological evidence highlighting the PAG as an important subcortical area in the neural circuitry of the cardiorespiratory response to exercise, since stimulation of this structure is known to alter blood pressure in awake humans.

High cardiorespiratory fitness in early to late middle age preserves the cortical circuitry associated with brain-heart integration during volitional exercise

Journal of Neurophysiology, 2017

This study tested the hypothesis that high cardiorespiratory fitness (peak oxygen uptake) preserves the cortical circuitry associated with cardiac arousal during exercise in middle- to older-aged individuals. Observations of changes in heart rate (HR) and in cortical blood oxygenation level-dependent (BOLD) images were made in 52 healthy, active individuals (45–73 yr; 16 women, 36 men) across a range of fitness (26–66 ml·kg−1·min−1). Seven repeated bouts of isometric handgrip (IHG) at 40% maximal voluntary contraction force were performed with functional magnetic resonance imaging at 3 T, with each contraction lasting 20 s and separated by 40 s of rest. HR responses to IHG showed high variability across individuals. Linear regression revealed that cardiorespiratory fitness was not a strong predictor of the HR response ( r2 = 0.09). In a region-of-interest analysis both the IHG task and the HR time course correlated with increased cortical activation in the bilateral insula and decre...

The relevance of central command for the neural cardiovascular control of exercise

2010

This paper briefly reviews the role of central command in the neural control of the circulation during exercise. While defined as a feedfoward component of the cardiovascular control system, central command is also associated with perception of effort or effort sense. The specific factors influencing perception of effort and their effect on autonomic regulation of cardiovascular function during exercise can vary according to condition. Centrally mediated integration of multiple signals occurring during exercise certainly involves feedback mechanisms, but it is unclear whether or how these signals modify central command via their influence on perception of effort. As our understanding of central neural control systems continues to develop, it will be important to examine more closely how multiple sensory signals are prioritized and processed centrally to modulate cardiovascular responses during exercise. The purpose of this article is briefly to review the concepts underlying central command and its assessment via perception of effort, and to identify potential areas for future studies towards determining the role and relevance of central command for neural control of exercise.

Application of positron emission tomography to neuroimaging in sports sciences

Methods, 2008

To investigate exercise-induced regional metabolic and perfusion changes in the human brain, various methods are available, such as positron emission tomography (PET), functional magnetic resonance imaging (fMRI), near-infrared spectroscopy (NIRS) and electroencephalography (EEG). In this paper, details of methods of metabolic measurement using PET, [ 18 F]fluorodeoxyglucose ([ 18 F]FDG) and [ 15 O]radio-labelled water ([ 15 O]H 2 O) will be explained. Functional neuroimaging in the field of neuroscience was started in the 1970s using an autoradiography technique on experimental animals. The first human functional neuroimaging exercise study was conducted in 1987 using a rough measurement system known as 133 Xe inhalation. Although the data was useful, more detailed and exact functional neuroimaging, especially with respect to spatial resolution, was achieved by positron emission tomography. Early studies measured the cerebral blood flow changes during exercise. Recently, PET was made more applicable to exercise physiology and psychology by the use of the tracer [ 18 F]FDG. This technique allowed subjects to be scanned after an exercise task is completed but still obtain data from the exercise itself, which is similar to autoradiography studies. In this report, methodological information is provided with respect to the recommended protocol design, the selection of the scanning mode, how to evaluate the cerebral glucose metabolism and how to interpret the regional brain activity using voxel-by-voxel analysis and regions of interest techniques (ROI). Considering the important role of exercise in health promotion, further efforts in this line of research should be encouraged in order to better understand health behavior. Although the number of research papers is still limited, recent work has indicated that the [ 18 F]FDG-PET technique is a useful tool to understand brain activity during exercise.

Coronary artery disease affects cortical circuitry associated with brain-heart integration during volitional exercise

Journal of Neurophysiology, 2015

This study tested the hypothesis that coronary artery disease (CAD) alters the cortical circuitry associated with exercise. Observations of changes in heart rate (HR) and in cortical blood oxygenation level-dependent (BOLD) images were made in 23 control subjects [control; 8 women; 63 ± 11 yr; mean arterial pressure (MAP): 90 ± 9 mmHg] (mean ± SD) and 17 similarly aged CAD patients (4 women; 59 ± 9 yr; MAP: 87 ± 10 mmHg). Four repeated bouts each of 30%, 40%, and 50% of maximal voluntary contraction (MVC) force (LAB session), and seven repeated bouts of isometric handgrip (IHG) at 40% MVC force (fMRI session), were performed, with each contraction lasting 20 s and separated by 40 s of rest. There was a main effect of group ( P = 0.03) on HR responses across all IHG intensities. Compared with control, CAD demonstrated less task-dependent deactivation in the posterior cingulate cortex and medial prefrontal cortex, and reduced activation in the right anterior insula, bilateral precentr...

The initial phase of exercise hyperpnoea in humans is depressed during a cognitive task

Experimental Physiology, 2005

Increased wakefulness is known to suppress the initial ventilatory response to passive movement and the steady-state ventilatory response to exercise. However, the effect of increased wakefulness upon the integrated ventilatory response at the onset of exercise is not known. We hypothesized that increasing wakefulness via a cognitive task would attenuate the initial ventilatory response to exercise, and so we examined the response to active leg extensions under two conditions: with and without concurrently solving a puzzle. At rest before exercise, subjects demonstrated greater minute ventilation while solving a puzzle (mean ± S.E.M., 12.38 ± 0.55 versus 10.12 ± 0.51 l min −1 , P < 0.001), due to a higher mean breathing frequency (mean ± S.E.M., 17.1 ± 0.93 versus 13.6 ± 0.59 breaths min −1 , P < 0.001). At the start of exercise, subjects did not increase their ventilation significantly while solving the puzzle (P = 0.170), but did by a mean ± S.E.M. of 6.16 ± 1.12 l min −1 (P < 0.001) when not puzzle solving. The ventilation achieved at the start of exercise in absolute terms was also lower while solving the puzzle . Despite differences in the rapid ventilatory response to exercise between conditions, the steady-state responses were not different. We conclude that the performance of a cognitive task decreases the initial phase of exercise hyperpnoea, and suggest that this might occur because of either a competitive interaction between drives to breathe or a behavioural distraction from the 'task' of exercise.

Cerebral correlates of autonomic cardiovascular arousal: a functional neuroimaging investigation in humans

The Journal of Physiology, 2000

Exercise, mental effort and emotional states are accompanied by reproducible changes in peripheral cardiovascular function affecting regional and systemic perfusion. The sympathetic and parasympathetic axes of the autonomic nervous system act to produce these integrated cardiovascular response patterns necessary for the metabolic support of behaviour, and are controlled directly by central autonomic nuclei within the brainstem and cerebellum. These autonomic regions receive afferent inputs from cortical and subcortical systems implicated in emotional and volitional behaviours. Peripheral autonomic responses may be an integral component of learning within cortical and subcortical systems (apparent in classical fear conditioning), and feedback of such responses may also influence emotional behaviour and decision making (Damasio et al. 1991). There is, as yet, only limited understanding of how 'higher' brain areas control and represent altered peripheral autonomic states in humans. Studies in experimental animals have helped to identify components of the 'central autonomic network' and have enhanced our understanding of the functional relationships between cortical and subcortical centres in cardiovascular control (reviewed in Cechetto & Saper, 1990; Bennarroch, 1997). Changes in heart rate and blood pressure have been reported to result from electrical or chemical stimulation of

Brain Mapping the Effects of Chronic Aerobic Exercise in the Rat Brain Using FDG PET

Journal of Personalized Medicine

Exercise is a key component to health and wellness and is thought to play an important role in brain activity. Changes in brain activity after exercise have been observed through various neuroimaging techniques, such as functional magnetic resonance imaging (fMRI) and positron emission tomography (PET). The precise impact of exercise on brain glucose metabolism (BGluM) is still unclear; however, results from PET studies seem to indicate an increase in regional metabolism in areas related to cognition and memory, direction, drive, motor functions, perception, and somatosensory areas in humans. Using PET and the glucose analog [18F]-Fluorodeoxyglucose (18F-FDG), we assessed the changes in BGluM between sedentary and chronic exercise in rats. Chronic treadmill exercise treatment demonstrated a significant increase in BGluM activity in the following brain regions: the caudate putamen (striatum), external capsule, internal capsule, deep cerebellar white matter, primary auditory cortex, f...

Neural regulation of cardiovascular response to exercise: role of central command and peripheral afferents

BioMed research international, 2014

During dynamic exercise, mechanisms controlling the cardiovascular apparatus operate to provide adequate oxygen to fulfill metabolic demand of exercising muscles and to guarantee metabolic end-products washout. Moreover, arterial blood pressure is regulated to maintain adequate perfusion of the vital organs without excessive pressure variations. The autonomic nervous system adjustments are characterized by a parasympathetic withdrawal and a sympathetic activation. In this review, we briefly summarize neural reflexes operating during dynamic exercise. The main focus of the present review will be on the central command, the arterial baroreflex and chemoreflex, and the exercise pressure reflex. The regulation and integration of these reflexes operating during dynamic exercise and their possible role in the pathophysiology of some cardiovascular diseases are also discussed.

Central activation of autonomic effectors during mental simulation of motor actions in man.

1993

Abstract 1. Healthy subjects actually performed and mentally simulated a leg exercise at two levels of work (15 and 19 kg loads). Heart rate, respiration rate and end-tidal PCO2 were measured in both conditions. In addition, muscular metabolism was simultaneously measured using 31P nuclear magnetic resonance (NMR) spectroscopy. 2. During actual exercise, heart and respiration rates increased, first abruptly and then gradually in relation to the level of work. End-tidal PCO2 was unaltered.