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 degrees 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 degrees 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 degrees 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.

Figure 1. Cat cortical loci activated by phrenic nerve afferents

The left panel is a photograph of the rostral cat cerebral cortex. The PCD is the location of the post-cruciate dimple. The right panel is a schematic representation of the sensorimotor, pericruciate region of the cat cerebral cortex. Each filled circle represents to cortical surface location of the 1° CEP for an individual animal. The shaded oval is the cortical area that contains more than 75% of the 1° CEP loci.

Figure 2. Cerebral cortical surface 1° CEP elicited by electrical stimulation of the whole phrenic nerve intrathoracically for an individual animal

The onset and peak latencies are indicated.

Figure 4. Bilateral cat cortical loci activated by phrenic nerve afferents

The top panels are the rostral cat cerebral cortex schematic representation of the sensorimotor, pericruciate region. The 1° CEP was recorded contralateral and ipsilateral to whole phrenic nerve stimulation intrathoracically. Each filled circle represents the cortical surface location of the 1° CEP for an individual animal. The bottom panel is a 1° CEP from an individual animal with the contralateral and ipsilateral cerebral cortical CEP recorded simultaneously.

Figure 3. Photograph of an histological saggital section through the rostral cerebral cortex of an individual animal

The arrows indicate the lesion made at the 1° CEP locus elicited by whole phrenic nerve stimulation intrathoracically. The architechtonic areas of this region of the cerebral cortex are indicated (Hassler & Muhs-Clement, 1964).

Figure 6. The 1° CEPs with bilateral phrenic nerve stimulation for an individual animal

The 1° CEPs recorded and elicited in the cerebral cortex contralateral to the phrenic nerve stimulated. The top trace is the 1° CEP recorded in the left cerebral cortex and elicited by stimulation right whole phrenic nerve intrathoracically. The middle trace was recorded at the same cerebral cortical site as the top trace with the 1° CEP elicited by stimulation of the C5 rootlet of the right phrenic nerve. The bottom trace is the 1° CEP recorded in the right cerebral cortex an elicited by stimulation left whole phrenic nerve intrathoracically.

Figure 5. Cat cortical loci activated by stimulation of C5 rootlet phrenic nerve afferents

The inset panel is a schematic representation of the sensorimotor, pericruciate region of the cat cerebral cortex with each filled circle representing the cortical surface location of the C5 phrenic 1° CEP for an individual animal.

Figure 7. Cat cortical loci activated by inspiratory occlusion

The left panel is the 1° CEP elicited by repeated single breath occlusions in an individual animal. The right panel is a schematic representation of the sensorimotor, pericruciate region of the cat cerebral cortex with each filled circle representing the cortical surface location of the inspiratory occlusion-elicited 1° CEP for an individual animal. The open circles are the 1° CEP for whole phrenic nerve stimulation in the same animals. The shaded oval is the cortical area that contains more than 75% of the phrenic nerve-elicited 1° CEP loci from Fig. 1.

Figure 8. Somatosensory cortical neuronal response to contralateral whole phrenic nerve stimulation

A is a short-latency cortical neuron activated by intrathoracic stimulation of the contralateral whole phrenic nerve. B is a recording from a different animal of 2 neurons, short- and long-latency activated by intrathoracic stimulation of the contralateral whole phrenic nerve.

Figure 9. Cat cortical 1° CEP loci activated by stimulation of forelimb, hindlimb and visceral nerve afferents

This is a schematic representation of the sensorimotor, pericruciate region of the cat cerebral cortex. Each number represents a cortical surface location of the 1° CEP for an individual animal for each nerve stimulated. Forelimb nerves were the cutaneous superficial radial (2) and muscle deep radial (3) nerves. The hindlimb nerves were the cutaneous sural (6) and muscle medial gastrocnemius (7) nerves. The thoracic mixed cutaneous and muscle intercostal nerve is indicated as 4. The visceral major splanchnic nerve is indicated as 5. The shaded oval is the cortical area that contains more than 75% of the 1° CEP loci from Fig. 1.