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. 2018 May 29:9:638.
doi: 10.3389/fphys.2018.00638. eCollection 2018.

Cerebral Ischemia Changed the Effect of Metabosensitive Muscle Afferents on Somatic Reflex Without Affecting Thalamic Activity

Caroline Pin-Barre  1 , Christophe Pellegrino  2 , Frédéric Laurin  3 , Jérôme Laurin  1
Affiliations

Cerebral Ischemia Changed the Effect of Metabosensitive Muscle Afferents on Somatic Reflex Without Affecting Thalamic Activity

Caroline Pin-Barre et al. Front Physiol. .

Abstract

The purpose of the present study was to examine the contribution of group III and IV metabosensitive afferents at spinal and supraspinal levels in rats subjected to middle cerebral artery occlusion (MCAO) with reperfusion during the acute phase. Animals were randomized in Control (n = 23), SHAM (n = 18), MCAO-D1 (n = 10), and MCAO-D7 (n = 20) groups. Rats performed the Electrical Von Frey and the Adhesive removal tests before the surgery and at day 1 (D1), D3, and D7 after MCAO. Animals were subjected to electrophysiological recordings including the responses of group III/IV metabosensitive afferents to combinations of chemical activators and the triceps brachii somatic reflex activity at D1 or D7. The response of ventral posterolateral (VPL) thalamic nuclei was also recorded after group III/IV afferent activation. Histological measurements were performed to assess the infarct size and to confirm the location of the recording electrodes into the VPL. Behavioral results indicated that MCAO induced disorders of both mechanical sensibility and motor coordination of paretic forepaw during 7 days. Moreover, injured animals exhibited an absence of somatic reflex inhibition from the group III/IV afferents at D1, without affecting the response of both these afferents and the VPL. Finally, the regulation of the central motor drive by group III/IV afferents was modified at spinal level during the acute phase of cerebral ischemia and it might contribute to the observed behavioral disturbances.

Keywords: mechanical sensibility; somatic reflex; spinal plasticity; stroke recovery; thalamus dysfunction.

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Figures

FIGURE 1
FIGURE 1
Experimental protocol during 7 days post-MCAO and electrophysiological procedures. (A) Electrophysiological recordings at the spinal cord or VPL levels were performed at day 1 (D1) or day 7 (D7) post-MCAO before histological analysis. Moreover, animals sacrificed at D7 also carried out the behavioral tests at D1, D3, and D7. (B) Experimental procedures for the somatic reflex recording evoked at the C7 dorsal root (top right), the recording of afferent firing rate at the C7 dorsal root (bottom left) and for the recording of both VPL nuclei firing rate (bottom right). α-Mn: α-motoneurons; C7: cervical 7.
FIGURE 2
FIGURE 2
Changes in somatic reflex response following (A) KCl 10-LA 25, (B) LA 25-ATP, and (C) KCl 50-LA 50 injections in the triceps brachii. Values are expressed in the percentage (%) of PRE amplitude reflex. ∗p < 0.05, ∗∗p < 0.01: PRE-injections vs. POST-injections in Control, SHAM, MCAO-D1, and MCAO-D7 groups; + p < 0.05: MCAO-D1 vs. Control and SHAM groups. (D) Examples of somatic reflex responses to metabosensitive afferent stimulations between SHAM and MCAO-D1 groups. The amplitude of the somatic reflex was not modified following chemical activator injections for MCAO-D1 animal unlike the one of the SHAM animal.
FIGURE 3
FIGURE 3
Changes in the discharge of metabosensitive afferent after intra-arterial injection of chemical activators in the triceps brachii. (A) Values are expressed in the percentage (%) of firing rate baseline (PRE). ∗p < 0.05, ∗∗p < 0.01, ∗∗∗p < 0.001: POST-injections vs. PRE-injections in Control (n = 13), SHAM (n = 10), MCAO-D1 (n = 10), and MCAO-D7 (n = 14) groups. (B) Examples of metabosensitive afferents firing rate after KCl 50-LA 50 in rat of Control group.
FIGURE 4
FIGURE 4
Changes in ipsi- (IP) and contralesional (CT) VPL nuclei response following intra-arterial injection of chemical activators in the triceps brachii. (A) Values are expressed in IP-POST/IP-PRE and CT-POST/CT-PRE ratios in which PRE corresponded to VPL nuclei baseline in responses to saline injection. ∗p < 0.05, ∗∗p < 0.01, ∗∗∗p < 0.001: POST-injections vs. PRE-injections in Control (n = 10), SHAM (n = 8), and MCAO-D7 (n = 6) groups. ⊙p < 0.05: IP-POST/IP-PRE vs. CT-POST/CT-PRE in Control group after KCl 50-LA 50 injections only. (B) Example of IP and CT VPL nuclei firing rate after KCl 50-LA 50 from a Control rat. IP: ipsilesional; CT: contralesional.
FIGURE 5
FIGURE 5
PPADS injection reduced (A) somatic reflex and (B) metabosensitive afferent responses following chemical activator injections. Values are expressed in the percentage (%) of decrease compared to PRE-PPADS variation in additional animals (n = 5). ∗p < 0.05: POST-PPADS vs. PRE-PPADS.
FIGURE 6
FIGURE 6
Histological analysis. (A) Cresyl violet staining (top right picture) revealed that electrodes were located into VPL nucleus according to the Figure 52 of Paxinos and Watson (2006) (top left picture). In this schematic representation of coronal brain slice, VPL nucleus area was colored in orange. (B) TTC staining revealed infarct size (white-colored area) in whole brain slices at D1 and D7 after 2 h of MCAO surgery. (C) Affected brain regions by MCAO-induced ischemia. In our study, caudate nucleus (striatum) and primary somatosensory area of left forepaw (S1-LF) were affected by cerebral ischemia at D1 as well as at D7 according to Paxinos and Watson (2006) brain atlas. Nevertheless, the thalamus seemed to be intact at macroscopic level.
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