Trigeminal Sensory Supply Is Essential for Motor Recovery after Facial Nerve Injury
Abstract
:1. Clinical Importance of the Afferent Fibers, including Trigeminal Nerve Fibers, for Appropriate Motor Nerve Regeneration and Recovery of Motor Performance
2. Ablation of Trigeminal Sensory Input by Excising the Ipsilateral Infraorbital Nerve (IOn-ipsi-ex) Impedes Recovery of Vibrissae Motor Performance after Transection and Suture of the Facial Nerve (Fn-n). Manual Stimulation (Mstim) of the Paralyzed and Deafferented Whisker Pad Worsens Recovery of Whisking. See Flow Chart Table 2 for a Synopsis
2.1. Functional Recovery
Research Goals | Day 0 (Beginning) | Day 1: Surgeries | Day 2–63 (Two Months) | Day 64 (8 Weeks Later) | Day 65 (1 Day Later) | Day 75 (10 Days Later) | Results |
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Section 2: To determine recovery of vibrissae motor performance after transection and suture of the facial nerve (Fn-n), and after Ablation of trigeminal sensory input, by excising the ipsilateral infraorbital nerve (IOn-ipsi-ex). | Clipping of all vibrissal hairs except 2 on each side of the face in preparation for the videotaping. Pre-operative videotaping of 24 intact rats for video-based motion analysis of the vibrissae movements. | Right (Fn-n) in all 24 rats. 6 rats (group 1) received no other treatment. 6 rats received daily Mstim of the whisker pad (group 2). Another 6 rats received an excision of the ipsilateral infraorbital nerve (IOn-ipsi-ex) (group 3). The last 6 rats received Mstim in addition to Fn-n + IOn-ipsi-ex (group 4). | Daily manual stimulation of the whisker pad in groups 2 and 4. | Clipping of all vibrissal hairs except 2 on each side of the face in preparation for the videotaping. Postoperative videotaping of all 24 rats for video-based motion analysis of the vibrissae movements. | Perfusion fixation with 4% paraformaldehyde in phosphate-buffered saline, pH 7.4 | Cutting of the brainstems on a vibratome and determining the intensity of fluorescence after immunostaining for synaptophysin. Cutting of the ipsilateral to Fn-n levator labii superioris muscle (LLS) on a cryostat and determining the degree of polyinnervation of the motor endplates. | Amplitude: Intact: 62 ± 6° Fn-n: 19 ± 6° Fn-n + Mstim: 51 ± 19° Fn-n + IOn-ipsi-ex: 22 ± 3° Fn-n + Ion-ipsi-ex + Mstim: 14 ± 6° Polyinnervation %: Intact: 0% Fn-n: 53 ± 10%; Fn-n + Mstim: 22 ± 3%; Fn-n + Ion-ipsi-ex: 43 ± 9%; Fn-n + Ion-ipsi-ex + Mstim: 51 ± 10% |
2.2. Muscle Innervation
2.3. Conclusions
3. Mild Ipsilateral to Fn-n Trigeminal Indirect Stimulation (by Removing the Contralateral Vibrissal Hairs) and Direct Trigeminal Stimulation (by Massaging the Ipsilateral Whisker Pad) after Double Anastomotic Surgery on the Sensory Infraorbital and Motor Facial Nerves Improves the Quality of Muscle Reinnervation and Vibrissal Motor Performance. See Flow Chart Table 3 for a Synopsis
3.1. Experimental Rat Groups
Experiment’s Research Goals | Day 0 (Beginning) | Day 1: Surgeries (1 Day Later) | Day 2–111 | Day 64–111 | Day 112 | Day 113–118 | Results |
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Section 3: To determine the effect of mild trigeminal indirect stimulation of sensory nerves (by removing the contralateral vibrissal hairs and massaging the ipsilateral whisker pad), after double anastomotic surgery on the sensory infraorbital and motor facial nerve, on the quality of muscle reinnervation and vibrissal motor performance. | Clipping of all vibrissal hairs except 2 on each side of the face in preparation for the videotaping. Pre-operative videotaping of 48 intact rats for video-based motion analysis of the vibrissae movements. | Right Fn-n + IOn-n) in 48 rats. 12 rats (group 1) received no other treatment. In another 12 rats (group 2) the contralateral vibrissal hairs were removed (vibrissal stimulation; Fn-n + IOn-n + Vstim). In rats from group 3, the ipsilateral whisker pads were manually stimulated (Fn-n + IOn-n + Mstim). In rats from group 4, the Vstim of the reinnervated vibrissae was followed by Mstim (Fn-n + IOn-nN + Vstim + Mstim). | Daily manual stimulation of whisker pads in group 3. | Daily manual stimulation of whisker pads in group 4. | Clipping of all vibrissal hairs except 2 on each side of the face in preparation for videotaping. Postoperative videotaping of all rats for video-based motion analysis of the vibrissae movements. Injection of 1% Fast Blue to back-label motoneuronal perikarya. | Perfusion fixation with 4% PFA in 0.1 M PBS, pH 7.4 Cutting of the brainstems on a vibratome and determining the intensity of synaptophysin fluorescence. Cutting of the ipsilateral to Fn-n LLS on a cryostat and determining the degree of polyinnervation of the motor endplates. | Amplitude Intact: 62 ± 6°; Fn-n + IOn-n: 11 ± 4°; Fn-n + IOn-n + Vstim: 28 ± 9°; Fn-n + IOn-n + Mstim: 30 ± 11°; Fn-n + Ion-n + Vstim +Mstim: 32 ± 10°. Polyinnervation %: Intact: 0%; Fn-n + IOn-n: 58 ± 8%; Fn-n + IOn-n + Vstim: 40 ± 3%; Fn-n + IOn-n + Mstim: 40 ± 2%; Fn-n + IOn-n + Vstim + Mstim: 33 ± 10%. Synaptophysin covered area:: Intact: 17 ± 2%; Fn-n + IOn-n: 12 ± 1%; Fn-n + IOn-n + Vstim: 13 ± 2% Fn-n + IOn-n + Mstim: 13 ± 2%; Fn-n + IOn-n + Vstim + Mstim: 12 ± 2%. |
3.2. Functional Recovery
3.3. Morphological Estimates in the Facial Muscles
3.4. Morphological Estimates in the Facial Nucleus
3.5. Conclusions
3.6. Clinical Application
4. Intensive Ipsilateral to Fn-n Trigeminal Indirect Stimulation, Produced by Its Forced Overuse Due to Excision of the Contralateral Infraorbital Nerve (Ion) after Surgery on the Buccal Branch of the Facial Nerve, Attenuates the Degree of Collateral Axonal Branching. See Flow Chart Table 4 for a Synopsis
4.1. Introduction
Experimental Set Research Goals | Day 1: Surgeries | Day 28 (4 Weeks Later) | Day 38 (10 Days Later) | Day 38 | Results |
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Section 4: Effects of the intensive trigeminal indirect stimulation (excision of the contralateral infraorbital nerve) after surgery on the buccal branch of the facial nerve, on the degree of collateral axonal branching at the lesion site. | All groups of rats consisted of 6 animals. Rats in group 1 served as unoperated controls. Rats in groups 2–4 were subjected to identical transection and suture of the right buccal branch of the facial nerve (buccal–buccal anastomosis, Bn-n). The rats of group 3 underwent Bn-n plus excision of the ipsilateral (right) IOn (Bn-n + IOn-ipsi-ex), and those of group 4 underwent Bn-n plus excision of the contralateral (left) IOn (Bn-n + IOn-contra-ex). | Retrograde labeling of the facial motoneurons with fluorescent tracers, Fluoro-Gold (FG; Fluorochrome Inc., Englewood, CO, USA) and DiI (Molecular Probes, The Netherlands), applied to the superior and inferior buccolabial nerves (BLn) respectively. | Perfusion fixation with 4% paraformaldehyde in phosphate-buffered saline, pH 7.4 | Cutting of the brainstems on a vibratome and determining the number of double-labelled (FG + DiI) perikarya which indicates the degree of collateral axonal branching at the site of nerve injury. | Portion of double-labelled perikarya: Intact: 0%; Bn-n: 23%; Bn-n + IOn-ipsi-ex: 13%; Bn-n + IOn-contra-ex: 8% |
4.2. Identification and Localization of Facial Motoneurons Regenerating into the Branches of the Buccal Nerve after Bn-n Surgery
4.3. Results
4.3.1. Rat Group 1: Distribution of Facial Motoneurons in Both Branches of the Buccal Nerve in Unoperated Rats
4.3.2. Rat Group 2: Buccal–Buccal Anastomosis (Bn-n)
4.3.3. Rat Group 3: Bn-n Plus Excision of the Ipsilateral Infraorbital Nerve (IOn)
4.3.4. Rat Group 4: Bn-n Plus Excision of the Contralateral Infraorbital Nerve (IOn)
4.4. Conclusions
5. Intensive Ipsilateral to Fn-n Trigeminal Indirect Stimulation, Produced by Its Forced Overuse Due to Excision of the Contralateral Infraorbital Nerve (Ion) after Surgery on the Buccal Branch of the Facial Nerve, Improves the Accuracy of Muscle Reinnervation. See Flow Chart Table 5 for a Synopsis
5.1. Research Question
Experimental Set Research Goals | 10 Days before Surgery | Day 0: Surgeries | Day 28 (4 Weeks Later) | Day 38 (10 Days Later) | Day 38 | Results |
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Section 5: Effect of intensive trigeminal indirect stimulation (excision of the contralateral IOn) after surgery on Bn on the accuracy of muscle reinnervation. | Buccal motoneurons were back labelled prior to surgeries in all 4 rat groups (each of 6 rats) to identify and localize their motoneuronal perikarya in the brainstem. A solution of 1% Fluoro-Gold (FG) was injected into the muscles of the whisker pad. | Rats in group 1 served as unoperated controls. Rats in groups 2–4 were subjected to identical transection and suture of the right buccal branch of the facial nerve (buccal–buccal anastomosis, Bn-n). The rats of group 3 underwent Bn-n plus excision of the ipsilateral (right) IOn (Bn-n + IOn-ipsi-ex), and those of group 4 underwent Bn-n plus excision of the contralateral (left) IOn (Bn-n + IOn-contra-ex). | 28 days after surgery, a 1% solution of Fast Blue (FB) was injected into the same muscle site as the earlier FG injection. | Perfusion fixation with 4% paraformaldehyde in phosphate-buffered saline, pH 7.4 | Cutting of the brainstems on a vibratome and determining the number of double-labelled (FG + DiI) perikarya which indicates accuracy of muscle reinnervation. | Portion of double-labelled perikarya: Intact: ~90–100%; Bn-n: 27%; Bn-n + IOn-ipsi-ex: 32%; Bn-n + IOn-contra-ex: 41% |
5.2. Surgeries and Rat Groups
5.3. Identification and Localization of Buccal Motoneurons Regenerating into Muscles of the Whisker Pad
5.4. Results
5.4.1. Rat Group 1
5.4.2. Rat Group 2: Bn-n
5.4.3. Rat Group 3: Bn-n Plus Excision of the Ipsilateral IOn (Bn-n + IOn-ipsi-ex)
5.4.4. Rat Group 4: Bn-n Plus Excision of the Contralateral IOn (Group BBA + ION-Contra-ex)
5.5. Conclusions
5.6. Discussion
5.7. Clinical Implications
6. Direct Stimulation of the Trigeminal Nerve Afferents (by Manual Stimulation of the Whisker Pad, Massage) after Facial Nerve Surgery Restores the Synaptic Density in the Facial Nucleus, Improves the Quality of Target Reinnervation and Promotes Recovery of Vibrissal Motor Performance. See Flow Chart Table 6 for a Synopsis
6.1. Experimental Rationale
6.2. Methods
Experiment’s Research Goal | Day 0 (Beginning) | Day 1: Surgeries (1 Day Later) | Day 2–56 (2 Months) | Day 57 | Day 58–67 | Results |
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Section 6: Effect of direct stimulation of the trigeminal nerve afferents (by manual stimulation of the whisker pad, massage) after facial nerve surgery on the synaptic density in the facial nucleus. | Clipping of all vibrissal hairs except 2 on each side of the face in preparation for the videotaping. Pre-operative videotaping of all intact rats for video-based motion analysis of the vibrissae movements. | 6 animals in group 1 were intact controls. The facial nerve was cut and re-sutured (Fn-n) in the experimental groups 2 and 3. In group 2 (6 rats; Fn-n + handling), the rats were held in the experimenter’s hand, not receiving any stimulation of the vibrissal muscles. In group 3 (r rats), Fn-n was followed by manual stimulation of the whisker pad (Fn-n + Mstim). | Daily manual stimulation of whisker pads in group 3. | Clipping of all vibrissal hairs except 2 on each side of the face in preparation for videotaping. Postoperative videotaping of all rats for video-based motion analysis of the vibrissae movements. | Perfusion fixation with 4% PFA in 0.1 M PBS, pH 7.4 Cutting of the brainstems on a vibratome and determining the intensity of synaptophysin fluorescence Cutting of the ipsilateral to Fn-n levator labii superioris muscle (LLS) on a cryostat and determining the degree of polyinnervation of the motor endplates. | Amplitude Intact: 57 ± 13° Fn-n + handl: 19 ± 6°; Fn-n + Mstim: 51 ± 19°; Polyinnervation %: Intact: 0% Fn-n + handl: 53 ± 10%; Fn-n + Mstim: 22 ± 5%; Amount of synaptophysin-positive terminals in the facial nucleus: Intact: 34.3 × 106 ± 2.3 × 106; Fn-n + handl: 29.2 × 106 ± 1.8 × 106; Fn-n + Mstim: 33 × 106 ± 2.6 × 10 |
6.3. Results
6.3.1. Recovery of Whisking
6.3.2. Loss of Synapses in the Lesioned Facial Nucleus
6.4. Discussion
6.5. Mechanisms
7. Muscle Neurotrophic Factors Are Unlikely to Play a Role in the Reduced Polyneuronal Muscle Reinnervation by Manual Stimulation of the Denervated Whisker Pad (Mstim). See Flow Chart Table 7 for a Synopsis
7.1. Experimental Rationale and Questions
Experiment’s Research Goal | Day 0 (Beginning) | Day 1: Surgeries (1 Day Later) | Day 2–56 (2 Months) | Day 57 | Day 58–67 | Results |
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Section 7: To determine the role of muscle neurotrophic factors in the reduced polyneuronal muscle reinnervation by manual stimulation of the denervated whisker pad (Mstim) | Clipping of all vibrissal hairs except 2 on each side of the face in preparation for the videotaping. Pre-operative videotaping of all intact rats for video-based motion analysis of the vibrissae movements. | 6 animals of group 1 were intact controls. The facial nerve was cut and re-sutured (Fn-n) in the experimental groups 2 and 3. In group 2 (6 rats, Fn-n + handling), the rats were held in the experimenter’s hand, not receiving any stimulation of the vibrissal muscles. In group 3, (6 rats) Fn-n was followed by manual stimulation of the whisker pad (Fn-n + Mstim). | Daily manual stimulation of whisker pads in group 3. | Clipping of all vibrissal hairs except 2 on each side of the face in preparation for videotaping. Postoperative videotaping of all rats for video-based motion analysis of the vibrissae movements. | Blood rinse by 0.1 M PBS, pH 7.4. Samples from LLS were taken and frozen. The translation of the proteins FGF2, IGF1 and NGF was determined using sandwich ELISA-Kits following the manufacturer’s instructions. | FGF2 Intact: 75 ± 16 pg/mg, FGF2 Fn-n+ handling: 69 ± 24 pg/mg FGF2 Fn-n + Mstim: 56 ± 11 pg/mg IGF1 Intact: 1492 ± 87 pg/mg IGF1 Fn-n + handling 2079 ± 300 pg/mg, IGF1 Fn-n + Mstim: 1821 ± 784 pg/mg NGF Intact: 61 ± 22 pg/mg NGF Fn-n + handling: 51 ± 21 pg/mg NGF Fn-n + Mstim: 33 ± 13 pg/mg. |
7.2. Methods
7.3. Results
7.4. Conclusions
8. Conclusions and Future Directions
Funding
Institutional Review Board Statement
Informed Consent Statement
Acknowledgments
Conflicts of Interest
List of Abbreviations
Nerves and muscles | |
BLn | buccolabial nerve |
Bn | buccal nerve (more correct: buccal branch of the facial nerve, ramus buccalis, motor) |
Fn | facial nerve (motor) |
IOn | infraorbital nerve (sensory) |
LLS | levator labii superioris muscle |
NMJ | neuromuscular junction |
Surgeries and procedures | |
Bn-n | buccal nerve transection and end-to-end suture (anastomosis) |
Fn-n | facial nerve transection and suture (anastomosis) |
Fn-n + Hand | facial nerve transection and suture plus handling |
IOn-contra-ex | excision of the contralateral infraorbital nerve |
IOn-ipsi-ex | excision of the ipsilateral infraorbital nerve |
IOn-n | infraorbital nerve transection and suture (anastomosis) |
Mstim | manual stimulation, massage |
Vstim | vibrissal stimulation |
Occ | occipital direction |
OP-side | operation side |
Dyes | |
DiI | 1,1′-dioctadecyl-3,3,3′,3′-tetramethylindo-carbocyanine perchlorate |
FB | Fast Blue |
FG | Fluoro-Gold |
Statistics | |
SD | standard deviation |
n | number |
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Section 2 (2 months) | Whisking Amplitude | NMJ Polyinnervation | ||
Rat groups | ||||
INTACT | 62 ± 6° | 0% | ||
Fn-n | 19 ± 6° | 53 ± 10% | ||
Fn-n + Mstim | 51 ± 19° | 22 ± 3% | ||
Fn-n + IOn-ipsi-ex | 22 ± 3° | 43 + 9% | ||
Fn-n + IOn-ipsi-ex + Mstim | 14 ± 6° | 51 ± 10% | ||
Section 3 (4 months) Rat Groups | Whisking Amplitude | NMJ Polyinnervation | Facial Motoneurons Perisomatic Terminal Fractional Area | |
INTACT | 62 ± 6° | 0% | 17 ± 2% | |
Fn-n + IOn-n | 11 ± 4° | 58 ± 8% | 12 ± 1% | |
Fn-n + IOn-n + Vstim | 28 + 9° | 40 ± 3% | 13 ± 2% | |
Fn-n + IOn-n + Mstim | 30 ± 11° | 40 ± 2% | 13 ± 2% | |
Fn-n + IOn-n + Vstim + Mstim | 32 ± 10° | 33 ± 10% | 12 ± 2% | |
Section 4 (4 weeks) | Buccal Branch Pathfinding | Buccal Branch Pathfinding | Buccal Branch Pathfinding | |
Rat groups | Superior-FG | Inferior-DiI | Sup + Inferior | |
INTACT | 91% | 9% | 0% | |
Bn-n | 56% | 21% | 23% | |
Bn-n + ipsi IOn-ex | 48% | 39% | 13% | |
Bn-n + contr IOn-ex | 69% | 23% | 9% | |
Section 5 (4 weeks) Rat Groups | Accuracy of Whisker pad Reinnervation | |||
INTACT | 100% | |||
Bn-n | 27% | |||
Bn-n + ipsi IOn-ex | 32% | |||
Bn-n + contr IOn-ex | 41% | |||
Section 6 (2 months) Rat Groups | Whisking Amplitude | LLS Polyinnervation of NMJ | Terminal Density (×106) on Facial Motoneurons | |
INTACT | 57 ± 13° | 0% | 34.3 ± 2.3 | |
Fn-n + Handling | 19 + 6° | 53 ± 10% | 29.2 ± 1.8 | |
Fn-n + Mstim | 51 ± 19° | 22 ± 5% | 33 ± 2.6 | |
Section 7 (2 months) Rat Groups | FGF2 Protein pg/mg | IGF1 Protein pg/mg | NGF Protein pg/mg | |
INTACT | 75 ± 16 | 1492 ± 87 | 61 ± 22 | |
Fn-n + Handling | 69 ± 24 | 2079 ± 300 | 51 ± 21 | |
Fn-n + Mstim | 56 ± 11 | 1821 ± 784 | 33 ± 13 |
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Rink-Notzon, S.; Reuscher, J.; Nohroudi, K.; Manthou, M.; Gordon, T.; Angelov, D.N. Trigeminal Sensory Supply Is Essential for Motor Recovery after Facial Nerve Injury. Int. J. Mol. Sci. 2022, 23, 15101. https://doi.org/10.3390/ijms232315101
Rink-Notzon S, Reuscher J, Nohroudi K, Manthou M, Gordon T, Angelov DN. Trigeminal Sensory Supply Is Essential for Motor Recovery after Facial Nerve Injury. International Journal of Molecular Sciences. 2022; 23(23):15101. https://doi.org/10.3390/ijms232315101
Chicago/Turabian StyleRink-Notzon, Svenja, Jannika Reuscher, Klaus Nohroudi, Marilena Manthou, Tessa Gordon, and Doychin N. Angelov. 2022. "Trigeminal Sensory Supply Is Essential for Motor Recovery after Facial Nerve Injury" International Journal of Molecular Sciences 23, no. 23: 15101. https://doi.org/10.3390/ijms232315101