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. 2019 Jan:216:51-58.
doi: 10.1016/j.autneu.2018.09.004. Epub 2018 Sep 15.

Direct neurophysiological evidence for a role of the human anterior cingulate cortex in central command

Martin J Gillies  1 , Yongzhi Huang  2 , Jonathan A Hyam  3 , Tipu Z Aziz  4 , Alexander L Green  4
Affiliations

Direct neurophysiological evidence for a role of the human anterior cingulate cortex in central command

Martin J Gillies et al. Auton Neurosci. 2019 Jan.

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: Anterior cingulate cortex; Cardiovascular system; Deep brain stimulation; Electrophysiology; Local field potentials; Motor system.

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Figures

Figure 1
Figure 1
Schematic of deep brain electrodes within the dorsal anterior cingulate cortex mapped onto a midline sagittal Montreal Neurological Institute brain template. Electrodes are scaled to size and electrode-neural interface contacts are shown in dark grey.
Figure 2
Figure 2
Graph to show change in mean heart rate during Rest, Anticipation and Exercise (confidence intervals represent standard error).
Figure 3
Figure 3
Local field potential power spectral density during Anticipation of exercise (pink lines) versus Rest (black lines) from 102 electrode channel recordings: A) across all frequencies; B) within the 25-60Hz band only, where increased synchronisation is seen during Anticipation.
Figure 4
Figure 4
Local field potential power spectral density during Exercise (green lines) versus Rest (black lines) from 102 electrode channel recordings: A) across all frequencies; B) within 6-14Hz range only. A desynchronisation during Exercise is seen in the 8-12Hz band compared to Rest.
Figure 5
Figure 5
Graph to show local field potential power spectral density changes between Rest, Anticipation and Exercise divided into frequency bands (* p<0.01).
Figure 6
Figure 6
Scatter plot to show the correlation: A) between heart rate and local field potential power in 25-60 Hz during Rest; B) between heart rate and local field potential power in 25-60 Hz during Anticipation; C) between the changes in heart rate and changes in local field potential power in 25-60 Hz during Anticipation relative to Rest (R=0.417, p=0.016); D) between heart rate and local field potential power in 8-12 Hz during Rest; E) between heart rate and local field potential power in 8-12 Hz during Exercise; F) between the changes in heart rate and changes in local field potential power in 8-12 Hz during Exercise relative to Rest.
Figure 7
Figure 7
Scatter plot to show the correlation: A) between SDNN and local field potential power in 8-12 Hz during Rest; B) between SDNN and local field potential power in 8-12 Hz during Exercise; C) between the changes in SDNN and changes in local field potential power in 8-12 Hz during Exercise relative to Rest.
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