Identification and Classification of Tongue-Innervating Mechanoreceptors
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Learn more at: https://insidescientific.com/webinar/identification-and-classification-of-tongue-innervating-mechanoreceptors/ Oral mechanosensory neurons provide essential information for feeding and social behaviors, yet no one knows the identities and functional properties of the neurons involved. Dr. Moayedi’s team identified anatomical classes of tongue-innervating neurons that express the mechanosensory ion channel Piezo2. These neurons are unique and do not fit into our understanding of mechanosensory neuron classes, making their role in sensation unclear. To address this, the team used in vivo calcium imaging of sensory neuron responses to tongue stimulation. They investigated responses of tongue-innervating trigeminal neurons to thermal and mechanical stimulation (e.g., pressure, brush, room temperature and cold fluid flow). In this webinar, Dr. Moayedi discusses her novel method to classify neuron response groups. These studies are amongst the first to classify mechanosensory neurons innervating the tongue.
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Identification and Classification of Tongue-Innervating Mechanoreceptors
- 1. Copyright 2022. All Rights Reserved. Contact Presenter for Permission Identification and classification of tongue- innervating mechanoreceptors Yalda Moayedi, PhD Departments of Neurology and Otolaryngology-Head & Neck Surgery Columbia University Assistant Professor
- 2. Identification and classification of tongue-innervating mechanoreceptors Yalda Moayedi, PhD Assistant Professor Departments of Neurology and Otolaryngology-Head & Neck Surgery
- 3. Eating is at the center of our lives
- 4. Mechanosensation is essential for oral functions Gap in knowledge: Mechanosensory cells and molecules that mediate oral behaviors in the healthy
- 5. Key questions 1. What are the anatomical substrates of oral mechanosensation? 2. What is the functional diversity of oral mechanosensory neurons? 3. How do alterations in mechanosensation impact function?
- 6. Somatosensory neurons are specialized to encode distinct sensory qualities shapes, textures sustained pressure pain, itch, sting, temperat ure flutter, vibration Zimmerman, Bai, Ginty, 2014
- 7. Sensory papillae of the anterior tongue
- 8. Anatomy of the human fungiform papillae 250 µm Moayedi et al., 2021
- 9. Human fungiform papillae have Meissner-like endings Taste Cells (K20) Myelinated Neurons (NFH) All Neurons (BIII) 50 µm Moayedi et al., 2021
- 10. Meissner’s Corpuscles Encode Vibrations and Flutter • Myelinated, corpuscular end organ • Encodes sensations of: • Vibration • Flutter Moayedi et al., 2021
- 11. Fungiform papillae are innervated by myelinated intraepithelial fibers surrounding taste buds Myelinated Neurons (NFH) All Neurons (BIII) 25 µm Moayedi et al., 2021
- 12. Piezo2 All neurons Taste cells 25 µm Mechanotransduction machinery is expressed in neurons surrounding fungiform taste buds in mice 15 µm Myelinated neurons All neurons Human Mouse Moayedi et al., 2018 & 2021
- 13. Sensory papillae of the anterior tongue
- 14. Anatomy of the human filiform papillae 250 µm Moayedi et al., 2021
- 15. Human filiform papillae have multiple end bulbs of Krause 50 µm Myelinated Neurons (NFH) All Neurons (BIII) Moayedi et al., 2021
- 16. 25 µm Innervation of filiform papillae is conserved between humans & mice 50 µm Myelinated Neurons (NFH) All Neurons (BIII) Mouse Human 25 µm Schwann cells (Nestin) All Neurons (BIII) Moayedi et al., 2018 & 2021
- 17. 30 µm Piezo2 All neurons Piezo2 is expressed in mouse end bulbs of Krause Moayedi et al., 2018
- 18. Anterior tongue is packed with mechanosensory neurons Mouse Human Filiform Papillae Fungiform Papillae
- 19. The hard palate is essential for flavor perception & bolus formation What mechanoreceptors are present in the hard palate? YouTube @Michael Farnan
- 20. Human palate is innervated by corpuscles and Merkel cells 50 µm Merkel Cells (K20) Myelinated Neurons (NFH) Moayedi et al., 2021
- 21. 10 µm Merkel cells-neurite complexes line hard palate rugae and encode texture and pressure Merkel Cells (K20) Myelinated Neurons (NFH) All Neurons (BIII) • Mechanosensory Merkel cell and myelinated afferent. • Encodes sensations of: • Texture • Sustained pressure Moayedi et al., 2021
- 22. Hard palate rugae comprise a high acuity surface in mice and human Merkel Cells (K20) Myelinated Neurons (NFH) 50 µm Human 25 µm Mouse Moayedi et al., 2018 & 2021
- 23. 25 µm Mouse 25 µm Human Merkel Cells (K20) All Neurons (BIII) Hard palate rugae comprise a high acuity surface in mice and human Moayedi et al., 2018 & 2021
- 24. Hard palate rugae are anatomically specialized for high acuity touch Bautista & Lumpkin, 2011, Moayedi et al., 2018 Hard Palate
- 25. Somatosensory endings of oral epithelia are poised to encode pressure and textures Hard Palate Tongue
- 26. Key questions 1. What are the anatomical substrates of oral mechanosensation? 2. What is the functional diversity of oral mechanosensory neurons? 3. How do alterations in mechanosensation impact function?
- 27. Somatosensory neurons are specialized to encode distinct sensory qualities shapes, textures sustained pressure pain, itch, sting, temperat ure flutter, vibration Zimmerman, Bai, Ginty, 2014 pressure neural response pressure neural response Low threshold High threshold
- 28. Distinct low threshold mechanosensory neuron populations are present in the human tongue Trulsson & Essick 1997 Rapidly Adapting Slowly Adapting Force Neuronal Discharge Frequency Neuronal Response
- 29. Imaging platform for selective tongue activation GCaMP6f Vigene Biosciences Trigeminal Neuron Calcium Responses Tongue Stimulation
- 30. Wnt1Cre, RosaGCaMP6f Tongue innervating trigeminal neurons respond to pressure and cool flow Pressure Cold Flow Low Ca2+ High Ca2+ Moayedi et al., bioRxiv, 2022
- 31. Controlled stimulation of tongue reveals distinct sensory neuron populations in the trigeminal ganglia Baseline 440 mN 23ºC flow 4ºC flow N = 601 neurons from 17 Wnt1Cre ,RosaGCaMP6f mice Moayedi et al., bioRxiv, 2022
- 32. Controlled stimulation of tongue reveals distinct sensory neuron populations in the trigeminal ganglia Cold/Cool Pressure Polymodal 83% 8% 9% Moayedi et al., bioRxiv, 2022 N = 601 neurons from 17 Wnt1Cre ,RosaGCaMP6f mice Brown-Forsyth ANOVA P=0.0005 Dunnett’s T3 post-hoc
- 33. Do tongue-innervating trigeminal mechanoreceptors respond to different stimulus features?
- 34. N = 289 neurons from 11 Wnt1Cre ,RosaGCaMP6f mice Tongue-innervating mechanosensory neurons are functionally diverse Moayedi et al., bioRxiv, 2022
- 35. Tongue-innervating trigeminal mechanoreceptors display distinct responses to pressure How many functionally distinct populations of trigeminal tongue-innervating mechanoreceptors are there? Time △f/f
- 36. Molecular markers label subgroups of trigeminal somatosensory neurons Ret 100 µm Vglut3 100 µm Ntrk3 100 µm All neurons Moayedi et al., bioRxiv, 2022
- 37. Molecular markers identify unique groups of mechanosensory tongue- innervating neurons 15 10 5 0 Vglut3Cre △f/f RetCreERT2 Ntrk3CreERT2 50 100 0 150 200 250 300 350 400 450 Time (s) Neurons 50 100 150 200 250 300 20 40 60 80 40 80 120 160 Moayedi et al., bioRxiv, 2022
- 38. Clustering identified five unique groups of tongue-innervating trigeminal neurons to pressure N = 616 neurons 5% 43% 9% 38% 5% Moayedi et al., bioRxiv, 2022
- 39. Cluster 1 neurons have sustained responses that encode pressure Moayedi et al., bioRxiv, 2022 N = 28 neurons 5% 43% 9% 38% 5% R2=0.17, Slope= 0.33, P<0.0001 R2=0.19, Slope= 0.31, P<0.0001 NS
- 40. N = 267 neurons Cluster 2 neurons respond to pressure with transient dynamics encoding movement Moayedi et al., bioRxiv, 2022 5% 43% 9% 38% 5% R2=0.04, Slope= 0.07, P<0.0001 R2=0.006, Slope= -0.003, P=0.015 P<0.0001
- 41. N = 57 neurons Cluster 3 neurons display transient, high threshold responses to force and are likely high-threshold mechano-nociceptors Moayedi et al., bioRxiv, 2022 5% 43% 9% 38% 5% R2=0.54, Slope= 0.54, P<0.0001 R2=0.003, Slope= -0.003, P=0.006 P<0.0001
- 42. N = 231 neurons Cluster 4a neurons are brush sensitive and do not encode force Moayedi et al., bioRxiv, 2022 5% 43% 9% 38% 5% R2=0.02, Slope= 0.012, P=0.0002 R2=0.04, Slope= -0.005, P<0.0001 P<0.0001
- 43. N = 33 neurons Cluster 4b neurons have a sustained inhibition from pressure Moayedi et al., bioRxiv, 2022 5% 43% 9% 38% 5%
- 44. N = 616 neurons The majority of mechanosensory tongue-innervating trigeminal neurons are tuned to detect movement and do not encode force well Moayedi et al., bioRxiv, 2022 5% 43% 9% 38% 5% Pressure Brush Force encoding? +++ + ++ - -
- 45. Cell body size correlates with function in the somatosensory system Le Pichon & Chesler, 2014
- 46. Tongue-innervating mechanosensory neuron clusters are anatomically distinct Median, Kruskal-Wallis test Neuron Soma Size Moayedi et al., bioRxiv, 2022 N = 616 neurons 5% 43% 9% 38% 5%
- 47. Tongue-innervating mechanosensory neuron clusters are molecularly distinct Vglut3 X + + + + Ntrk3 + + X + + Ret + + + + X Moayedi et al., bioRxiv, 2022 N = 616 neurons 5% 43% 9% 38% 5%
- 48. Key questions 1. What are the anatomical substrates of oral mechanosensation? 2. What is the functional diversity of oral mechanosensory neurons? 3. How do alterations in mechanosensation impact function over the lifetime?
- 49. Feeding changes drastically over a lifespan Old Young How do oral mechanoreceptors change over time? Feeding abilities Oral discrimination Oral mechanical thresholds
- 50. Merkel cell density reduces with age Merkel Cell Afferent Adult Elderly N=3-4 mice Two-Way ANOVA Bonferroni Post-Hoc P<0.01 Moayedi et al., 2018 Adult Elderly
- 51. Wild type Atoh1CKO Merkel cells are required for oil preference Median, N=8-11 males, T test with Welch’s correction CK Tong, Y Moayedi, & EA Lumpkin, in preparation
- 52. Conclusions Tongue and hard palate are densely innervated by a variety of mechanosensory endings tuned for high acuity touch. Vast majority of mechanosensory neurons in the tongue respond best to moving stimuli. Unbiased clustering reveals five distinct groups of tongue-innervating mechanosensory neurons. Tongue-innervating neuron classes are anatomically, functionally, and molecularly distinct Mechanosensory endings simplify with ageing. Disruption of a class of mechanosensory cell impacts food choice.
- 53. Acknowledgements Funding Berrie Neuroscience of Obesity Initiative (in vivo studies) SPN, (formerly NESTEC), (Anatomical studies) Thompson Family Foundation NIH/NHLBI 1T32HL120826 NIH/NINDS R25NS076445 NIH/NINDS R01NS105241-01 NIH/NIDCD R21DC018898 Ellen A. Lumpkin Lucia Duenas-Bianchi Ben Hoffman Rachel Clary Chi-Kun Tong Yoshi Baba Danny Florez-Paz Theanne Griffith Blair Jenkins Kara Marshall Collaborators Oral Anatomy Nestle Flavor Perception Team Paulette Bernd, CUMC Pathology Alia Koch, CUMC Dentistry Joy Chen, CUMC Dentistry Mark Park, CUMC Dentistry In vivo imaging David Yarmolinsky, BCH Alexander Chesler Lab, NCCIH Greg Gerling, UVA Shan Xu, UVA Lumpkin Lab Moayedi Lab Anisa Seenauth Caroline Cole SENse Lab at UC Berekely Sophie Obayashi
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