Identification of higher brain centres that may encode the cardiorespiratory response to exercise in humans

Abstract

1. Positron emission tomography (PET) was used to identify the neuroanatomical correlates underlying 'central command' during imagination of exercise under hypnosis, in order to uncouple central command from peripheral feedback.2. Three cognitive conditions were used: condition I, imagination of freewheeling downhill on a bicycle (no change in heart rate, HR, or ventilation, V I ): condition II, imagination of exercise, cycling uphill (increased HR by 12 % and V I by 30 % of the actual exercise response): condition III, volitionally driven hyperventilation to match that achieved in condition II (no change in HR).3. Subtraction methodology created contrast A (II minus I) highlighting cerebral areas involved in the imagination of exercise and contrast B (III minus I) highlighting areas activated in the direct volitional control of breathing (n = 4 for both; 8 scans per subject). End-tidal P CO 2 (P ET,CO 2 ) was held constant throughout PET scanning.4. In contrast A, significant activations were seen in the right dorso-lateral prefrontal cortex, supplementary motor areas (SMA), the right premotor area (PMA), superolateral sensorimotor areas, thalamus, and bilaterally in the cerebellum. In contrast B, significant activations were present in the SMA and in lateral sensorimotor cortical areas. The SMA/PMA, dorso-lateral prefrontal cortex and the cerebellum are concerned with volitional/motor control, including that of the respiratory muscles.5. The neuroanatomical areas activated suggest that a significant component of the respiratory response to 'exercise', in the absence of both movement feedback and an increase in CO 2 production, can be generated by what appears to be a behavioural response.

Relationship between motor corticospinal excitability and ventilatory response during intense exercise

“…Therefore, the findings in the present study not only support the above concept (Amman et al 2013) but also suggest that effort-mediated ventilatory response during fatiguing IE cannot be explained by the conventional framework of central command that drives breathing via neural mechanisms consisting of parallel activation of motor and respiratory centers (Goodwin et al 1972;Heigenhauser et al 1983;Krogh and Lindhard 1913;Marcora et al 2008). Recent studies (Decety et al 1991;Thornton et al 2001;Williamson et al 2002Williamson et al , 2006Yunoki et al 2009) using a cognitive approach to dissociate peripheral neural signals from central command have suggested that central command-mediated response does not necessarily require parallel activation of central motor command. Thornton et al (2001) showed by using positron emission tomography (PET) that breathing during imagination of effortful exercise was increased with significant activations of the dorsolateral prefrontal cortex, supplementary motor areas, premotor area, and cerebellum.…”

“…Recent studies (Decety et al 1991;Thornton et al 2001;Williamson et al 2002Williamson et al , 2006Yunoki et al 2009) using a cognitive approach to dissociate peripheral neural signals from central command have suggested that central command-mediated response does not necessarily require parallel activation of central motor command. Thornton et al (2001) showed by using positron emission tomography (PET) that breathing during imagination of effortful exercise was increased with significant activations of the dorsolateral prefrontal cortex, supplementary motor areas, premotor area, and cerebellum. Likewise, Williamson et al (2002) localized the insular and anterior cingulate cortices as important brain sites related to cardiovascular response induced by imagined handgrip exercise with effort sense.…”

Mechanism and implications of hyperpnea exaggeration at the onset of exercise in mechanical hyperalgesia after eccentric exercise

“…In this paper, we do not address the difference in the origin of central command in the higher centers 4) . Recently, except for the concept of parallel activation of locomotion and respiration 31) , ventilatory response has been reported to be modulated by other neurogenic drives, e.g., imagined exercise 32,33) and arousal response in the limbic system 7) . We distinguish them from the conventional concept of central command 31) in this paper.…”

Breathing Frequency Changes at the Onset of Stepping in Human Infants

“…Feedforward mechanisms associated with the command to start walking can alter respiration (reviewed in Waldrop et al 1996), as shown by electrical or chemical stimulation of locomotor regions in the midbrain in anesthetized intact, or unanaesthetized decerebrate cats, including those in which afferent feedback was eliminated by paralysis of the muscles (DiMarco et al 1983;Eldridge et al 1981Eldridge et al , 1985. Neuroimaging in intact humans further suggests participation of the motor cortex in exercise-related hyperpnea (Fink et al 1995) even when there is no overt movement (Thornton et al 2001). Our results cannot directly address the importance of central feedforward mechanisms in these infants.…”