Abstract
Introduction
The role of the anterior cingulate cortex (ACC) is still controversial. The ACC has
been implicated in such diverse functions as cognition, arousal and emotion in addition
to motor and autonomic control. Therefore the ACC is the ideal candidate to orchestrate
cardiovascular performance in anticipation of perceived skeletal activity. The aim
of this experiment was to investigate whether the ACC forms part of the neural network
of central command whereby cardiovascular performance is governed by a top-down mechanism.
Methods & results
Direct local field potential (LFP) recordings were made using intraparenchymal electrodes
in six human ACC's to measure changes in neuronal activity during performance of a
motor task in which anticipation of exercise was uncoupled from skeletal activity
itself. Parallel cardiovascular arousal was indexed by electrocardiographic changes
in heart rate. During anticipation of exercise, ACC LFP power within the 25–60 Hz
frequency band increased significantly by 21% compared to rest (from 62.7 μV2/Hz (±SE 4.94) to 76.0μV2/Hz (±SE 7.24); p = 0.004). This 25–60 Hz activity increase correlated with a simultaneous heart rate
increase during anticipation (Pearson's r = 0.417, p = 0.016).
Conclusions/Significance
We provide the first invasive electrophysiological evidence to support the role of
the ACC in both motor preparation and the top-down control of cardiovascular function
in exercise. This further implicates the ACC in the body's response to the outside
world and its possible involvement in such extreme responses as emotional syncope
and hyperventilation. In addition we describe the frequency at which the neuronal
ACC populations perform these tasks in the human.
Keywords
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References
- Hetereogeneity in neuronal intrinsic properties: a possible mechanism for hub-like properties of the rat anterior cingulate cortex during network activity.eNeuro. 2017; 4
- Prefrontal cortical projections to longitudinal columns in the midbrain periaqueductal gray in macaque monkeys.J. Comp. Neurol. 1998; 401: 455-479
- Long-term results of deep brain stimulation of the anterior cingulate cortex for neuropathic pain.World Neurosurg. 2017; 106: 625-637
- Initial and sustained brain responses to threat anticipation in blood-injection-injury phobia.Neuroimage Clin. 2017; 13: 320-329
- The involvement of the anterior cingulate cortex in blood pressure control.Brain Res. 1985; 340: 71-77
- Central neural correlates of learned heart rate control during exercise: central command demystified.J. Appl. Physiol. 1997; 83: 1448-1453
- Cerebral correlates of autonomic cardiovascular arousal: a functional neuroimaging investigation in humans.J. Physiol. 2000; 523: 259-270
- Human cingulate cortex and autonomic control: converging neuroimaging and clinical evidence.Brain. 2003; 126: 2139-2152
- Anterior cingulate activity during error and autonomic response.NeuroImage. 2005; 27: 885-895
- Central mechanisms underlying short- and long-term regulation of the cardiovascular system.Clin. Exp. Pharmacol. Physiol. 2002; 29: 261-268
- Hearing and seeing meaning in noise: alpha, beta, and gamma oscillations predict gestural enhancement of degraded speech comprehension.Hum. Brain Mapp. 2018; 39: 2075-2087
- General anaesthesia: from molecular targets to neuronal pathways of sleep and arousal.Nat. Rev. Neurosci. 2008; 9: 370-386
- The skin conductance orienting response as an index of attention.Biol. Psychol. 1983; 17: 27-39
- Physiological responses to brain stimulation during limbic surgery: further evidence of anterior cingulate modulation of autonomic arousal.Biol. Psychiatry. 2009; 66: 695-701
- Brain systems for baroreflex suppression during stress in humans.Hum. Brain Mapp. 2012; 33: 1700-1716
- Ready and waiting: freezing as active action preparation under threat.Neurosci. Lett. 2016; 619: 182-188
- Identifying cardiorespiratory neurocircuitry involved in central command during exercise in humans.J. Physiol. 2007; 578: 605-612
- Neural signatures in patients with neuropathic pain.Neurology. 2009; 72: 569-571
- Frontal midline theta rhythm and mental activity.Psychiatry Clin. Neurosci. 1998; 52: 555-566
- Medial prefrontal cortex generates frontal midline theta rhythm.Neuroreport. 1999; 10: 675-679
- Resting state connectivity of the medial prefrontal cortex covaries with individual differences in high-frequency heart rate variability.Psychophysiology. 2016; 53: 444-454
- Somato-motor, autonomic and electrocorticographic responses to electrical stimulation of rhinencephalic and other structures in primates, cat, and dog; a study of responses from the limbic, subcallosal, orbito-insular, piriform and temporal cortex, hippocampus-fornix and amygdala.Acta Physiol. Scand. Suppl. 1951; 24: 1-262
- Respiratory and vascular responses in monkeys from temporal pole, insula, orbital surface and cingulate gyrus; a preliminary report.J. Neurophysiol. 1949; 12: 347-356
- Human forebrain activation by visceral stimuli.J. Comp. Neurol. 1999; 413: 572-582
- The regulation of respiration and circulation during the initial stages of muscular work.J. Physiol. 1913; 47: 112-136
- Thalamic and cortical mechanisms of attention suggested by recent positron emission tomographic experiments.J. Cogn. Neurosci. 1990; 2: 358-372
- Theoretical analysis of the local field potential in deep brain stimulation applications.PLoS One. 2013; 8e59839
- Activation of central sympathetic networks during innocuous and noxious somatosensory stimulation.NeuroImage. 2011; 55: 216-224
- Functional subdivisions within anterior cingulate cortex and their relationship to autonomic nervous system function.NeuroImage. 2004; 22: 1151-1156
- Sleep and arousal: thalamocortical mechanisms.Annu. Rev. Neurosci. 1997; 20: 185-215
- From threat to fear: the neural organization of defensive fear systems in humans.J. Neurosci. 2009; 29: 12236-12243
- Anticipation causes increased blood flow to the anterior cingulate cortex.Hum. Brain Mapp. 1996; 4: 103-112
- Prefrontal cortical projections to the hypothalamus in macaque monkeys.J. Comp. Neurol. 1998; 401: 480-505
- A real-time QRS detection algorithm.IEEE Trans. Biomed. Eng. 1985; 32: 230-236
- Beta- and gamma-band activity reflect predictive coding in the processing of causal events.Soc. Cogn. Affect. Neurosci. 2016; 11: 973-980
- Functional imaging of brain responses to pain. A review and meta-analysis (2000).Neurophysiol. Clin. 2000; 30: 263-288
- Autonomic effects on stimulating rostral portion of cingulate gyri in man.J. Neurophysiol. 1949; 12: 385-392
- Seeing the mind.Science. 1993; 262: 673-674
- Localization of cognitive operations in the human brain.Science. 1988; 240: 1627-1631
- A role for primate subgenual cingulate cortex in sustaining autonomic arousal.Proc. Natl. Acad. Sci. U. S. A. 2014; 111: 5391-5396
- High and low gamma EEG oscillations in central sensorimotor areas are conversely modulated during the human gait cycle.NeuroImage. 2015; 112: 318-326
- Brain activity during sympathetic response in anticipation and experience of pain.Hum. Brain Mapp. 2013; 34: 1768-1782
- Pyramidal control of heart rate and arterial pressure in cats.Arch. Ital. Biol. 1999; 137: 47-62
- Dorsal anterior cingulate cortex and the value of control.Nat. Neurosci. 2016; 19: 1286-1291
- Advances in functional and structural MR image analysis and implementation as FSL.NeuroImage. 2004; 23: S208-S219
- Thalamocortical oscillations in the sleeping and aroused brain.Science. 1993; 262: 679-685
- Identification of higher brain centres that may encode the cardiorespiratory response to exercise in humans.J. Physiol. 2001; 533: 823-836
- Sympathetic regulation and anterior cingulate cortex volume are altered in a rat model of chronic back pain.Neuroscience. 2017; 352: 9-18
- Dorsal anterior cingulate cortices differentially lateralize prediction errors and outcome valence in a decision-making task.Front. Hum. Neurosci. 2018; 12: 203
- Hypnotic manipulation of effort sense during dynamic exercise: cardiovascular responses and brain activation.J. Appl. Physiol. 2001; 90: 1392-1399
- Brain activation by central command during actual and imagined handgrip under hypnosis.J. Appl. Physiol. 2002; 92: 1317-1324
- Evidence for central command activation of the human insular cortex during exercise.J. Appl. Physiol. 2003; 94: 1726-1734
- New insights into central cardiovascular control during exercise in humans: a central command update.Exp. Physiol. 2006; 91: 51-58
- Theta-activity in anterior cingulate cortex predicts task rules and their adjustments following errors.Proc. Natl. Acad. Sci. U. S. A. 2010; 107: 5248-5253
- Bayesian analysis of neuroimaging data in FSL.NeuroImage. 2009; 45: S173-S186
- Frontal lobe lesions and electrodermal activity: effects of significance.Neuropsychologia. 1999; 37: 1227-1241
Article info
Publication history
Published online: September 14, 2018
Accepted:
September 14,
2018
Received in revised form:
August 10,
2018
Received:
April 18,
2018
Identification
Copyright
© 2018 Elsevier B.V. All rights reserved.
