Phrenic nerve afferent activation of neurons in the cat SI cerebral cortex

Abstract

Stimulation of respiratory afferents elicits neural activity in the somatosensory region of the cerebral cortex in humans and animals. Respiratory afferents have been stimulated with mechanical loads applied to breathing and electrical stimulation of respiratory nerves and muscles. It was hypothesized that stimulation of the phrenic nerve myelinated afferents will activate neurons in the 3a and 3b region of the somatosensory cortex. This was investigated in cats with electrical stimulation of the intrathoracic phrenic nerve and C 5 root of the phrenic nerve. The somatosensory cortical response to phrenic afferent stimulation was recorded from the cortical surface, contralateral to the phrenic nerve, ispilateral to the phrenic nerve and with microelectrodes inserted into the cortical site of the surface dipole. Short-latency, primary cortical evoked potentials (1 • CEP) were recorded with stimulation of myelinated afferents of the intrathoracic phrenic nerve in the contralateral post-cruciate gyrus of all animals (n = 42). The mean onset and peak latencies were 8.5 ± 5.7 ms and 21.8 ± 9.8 ms, respectively. The rostro-caudal surface location of the 1• CEP was found between the rostral edge of the post-cruciate dimple (PCD) and the rostral edge of the ansate sulcus, medio-lateral location was between 2 mm lateral to the sagittal sulcus and the lateral end of the cruciate sulcus. Histological examination revealed that the 1• CEP sites were recorded over areas 3a and 3b of the SI somatosensory cortex. Intracortical activation of 16 neurons with two patterns of neural activity was recorded: (1) short-latency, short-duration activation of neurons and (2) long-latency, long-duration activation of neurons. Short-latency neurons had a mean onset latency of 10.4 ± 3.1 ms and mean burst duration of 10.1 ± 3.2 ms. The short-latency units were recorded at an average depth of 1.7 ± 0.5 mm below the cortical surface. The long-latency neurons had a mean onset latency of 36.0 ± 4.2 ms and mean burst duration of 32.2 ± 8.4 ms. The long-latency units were recorded at an average depth of 2.4 ± 0.2 mm below the cortical surface. The results of the study demonstrated that phrenic nerve afferents have a short-latency central projection to the SI somatosensory cortex. The phrenic afferents activated neurons in lamina III and IV of areas 3a and 3b. The cortical representation of phrenic nerve afferents is medial to the forelimb, lateral to the hindlimb, similar to thoracic loci, hence the phrenic afferent SI site in the cat homunculus is consistent with body position (thoracic region) rather than spinal segment (C 5 -C 7 ). The phrenic afferent activation of the somatosensory cortex is bilateral, with the ipsilateral cortical activation occurring subsequent to the contralateral. These results support the hypothesis that phrenic afferents provide somatosensory information to the cerebral cortex which can be used for diaphragmatic proprioception and somatosensation.

Twitches, Blinks, and Fidgets: Important Generators of Ongoing Neural Activity

“…Respiration-related nuclei project to the locus coeruleus, and sighing can change arousal levels (Yackle and others 2017), but respiration by itself probably does not drive time-locked brain-wide electrical responses (Parabucki and Lampl 2017). As the somatosensory cortex receives sensory input from the phrenic nerve (Davenport and others 2010), movement of the torso during respiration may drive bilateral somatosensory activation, and slow modulation of respiration would cause corresponding slow variations in neural activity in the trunk and visceral representations in somatosensory cortex. The confounds of respiration on brain-wide BOLD signals (the so-called “global signal”) are well known (Birn and others 2008a; Birn and others 2008b; Birn and others 2009; Murphy and others 2013).…”

Cortical Sources of Respiratory Mechanosensation, Laterality, and Emotion: An MEG Study

“…This periphery unceasingly provides sensory information to the brain, which takes up its role in discriminative processing and affective processing of different types of stimuli, e.g., mechanical loads, bronchoconstriction, hyperinflation, and blood gas changes [ 3 , 4 ]. Although researchers do not fully understand all cortical and subcortical neural pathways involved in respiratory sensory processing, previous studies have provided evidence related to respiratory-related brain activations in both humans and animals [ 5 , 6 , 7 , 8 , 9 , 10 , 11 , 12 , 13 , 14 , 15 , 16 , 17 , 18 ]. For example, a respiratory-related evoked potential (RREP) was recorded in lamb cortex [ 10 ], and phrenic nerve stimulation elicited an evoked potential in cat cerebral cortex [ 15 ].…”

Cortical and Subcortical Neural Correlates for Respiratory Sensation in Response to Transient Inspiratory Occlusions in Humans

“…The RREP studies have suggested the cortical sources of the Nf peak are likely located at the frontal cortices, the sources for the P1 peak to be the somatosensory cortices, the sources for the N1 and P3 peaks to be the right lateral sensorimotor cortices and lateral parietal cortices, respectively (Davenport et al, 1996; Logie et al, 1998; Chan and Davenport, 2010; von Leupoldt et al, 2010). Although the RREP studies were unable to provide inferences for subcortical activation patterns in response to respiratory mechanical stimulus, previous animal studies have suggested that stimulation to the phrenic nerve and thalamus resulted in direct inputs to the 3a and 3b areas (Yates et al, 1994; Davenport et al, 2010). In the present study, we collected the functional magnetic resonance imaging (fMRI) data for spatial localizations.…”