hide
Free keywords:
-
Abstract:
Human fMRI studies suggest that the autonomic nervous system (ANS) interacts with a central autonomic network (CAN) that is anchored in the bilateral anterior insular, mid-cingulate and inferior parietal cortices. CAN integrity bears relevance to ANS dysregulation in neurological and psychiatric disorders. Establishing the existence of a homolog network in the macaque could greatly facilitate systems-level investigations into causal CAN-ANS dynamics. Here, we recorded electrocardiography (ECG) and respiration in an awake, trained rhesus macaque during contrast-agent enhanced, whole-brain, high-resolution fMRI with implanted phased-array coils (0.6 mm isotropic voxels at 3T). Time-resolved estimates of parasympathetically-mediated, high frequency heart rate variability (hfHRV) were extracted from ECG using a Maximal Overlap Discrete Wavelet Packet Transform, subsequently down-sampled to TR resolution (3 sec), normalized, and convolved with a hemodynamic response function. The convolved hfHRV time series were regressed on the fMRI time series, while accounting for respiratory and cardiac noise via RETROICOR modeling. HfHRV was robustly anti-correlated with a network that prominently included the bilateral dorsal anterior insula (dAI), posterior and mid-cingulate cortices, precentral gyrus, and central sulcus. Subcortically, the network included the bilateral thalamus and putamen (p < 0.05, FWE-corrected). To test whether the configuration of CAN connectivity with the left and right dAI depended on fluctuations in cardiovagal state, we used the dAI time series and HRV time series to perform a physio-physiological interaction analysis. This revealed that functional connectivity of the left (but not right) dAI with the posterior, middle and anterior cingulate cortices, and the bilateral ventral dysgranular insula depends on cardiovagal state (p < 0.001), concordant with a previously proposed leftward parasympathetic dominance model. The striking similarity of human and macaque CANs that (anti)correlate with time-resolved estimates of hfHRV suggests substantial evolutionary conservation. The identified CAN has regional specificity characterized by contributions from cingulo-operculo-insular and sensorimotor systems. This pattern of coactivation may be consistent with original conceptualizations of the salience network as serving a domain general role in coordinating autonomic, behavioral, and cognitive responses to homeostatically relevant internal and external events.
