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Abstract
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Neurosciences

Kombineret perifer nervestimulering og kontrollerbar pulsparameter transkraniel magnetisk stimulering til sonde sensorimotorisk kontrol og læring

Published: April 21, 2023
doi:
10.3791/65212
, ,
1Department of Kinesiology and Health Sciences,University of Waterloo

Summary

Kort-latens afferent inhibering (SAI) er en transkraniel magnetisk stimuleringsprotokol til sonde sensorimotorisk integration. Denne artikel beskriver, hvordan SAI kan bruges til at studere de konvergerende sensorimotoriske sløjfer i motorcortex under sensorimotorisk adfærd.

Abstract

Dygtig motorisk evne afhænger af effektivt at integrere sensorisk afferens i de relevante motoriske kommandoer. Afferent hæmning giver et værdifuldt værktøj til at undersøge den proceduremæssige og deklarative indflydelse på sensorimotorisk integration under dygtige motoriske handlinger. Dette manuskript beskriver metoden og bidragene fra kortlatensafferent hæmning (SAI) til forståelse af sensorimotorisk integration. SAI kvantificerer effekten af en konvergent afferent volley på den kortikospinale motorudgang fremkaldt af transkraniel magnetisk stimulering (TMS). Den afferente volley udløses af den elektriske stimulering af en perifer nerve. TMS-stimulus leveres til et sted over den primære motoriske cortex, der fremkalder et pålideligt motorfremkaldt respons i en muskel, der betjenes af den afferente nerve. Omfanget af hæmning i den motorfremkaldte respons afspejler størrelsen af den afferente volley, der konvergerer på motorcortex og involverer centrale GABAerge og kolinerge bidrag. Den kolinerge involvering i SAI gør SAI til en mulig markør for deklarative-proceduremæssige interaktioner i sensorimotorisk præstation og læring. For nylig er undersøgelser begyndt at manipulere TMS-strømretningen i SAI for at drille den funktionelle betydning af forskellige sensorimotoriske kredsløb i den primære motoriske cortex for dygtige motoriske handlinger. Evnen til at styre yderligere pulsparametre (f.eks. pulsbredden) med state-of-the-art kontrollerbar pulsparameter TMS (cTMS) har forbedret selektiviteten af de sensorimotoriske kredsløb, der undersøges af TMS-stimulus og givet mulighed for at skabe mere raffinerede modeller af sensorimotorisk kontrol og læring. Derfor fokuserer det nuværende manuskript på OR-vurdering ved hjælp af cTMS. De principper, der er skitseret her, gælder imidlertid også for SAI vurderet ved hjælp af konventionelle TMS-stimulatorer med fast pulsbredde og andre former for afferent hæmning, såsom langlatensafferent hæmning (LAI).

Introduction

Flere sensorimotoriske sløjfer konvergerer i motorcortex for at forme pyramidekanalfremspring til spinalmotorneuroner og interneuroner1. Hvordan disse sensorimotoriske sløjfer interagerer for at forme kortikospinale fremspring og motorisk adfærd forbliver imidlertid et åbent spørgsmål. Short-latency afferent inhibering (SAI) giver et værktøj til at undersøge de funktionelle egenskaber af konvergerende sensorimotoriske sløjfer i motorcortexudgang. SAI kombinerer motorisk kortikal transkraniel magnetisk stimulering (TMS) med elektrisk stimulering af den tilsvarende perifere afferente nerve.

TMS er en ikke-invasiv metode til sikkert at stimulere pyramidemotoriske neuroner transsynaptisk i den menneskelige hjerne 2,3. TMS indebærer at føre en stor, forbigående elektrisk strøm gennem en oprullet ledning placeret i hovedbunden. Den elektriske strøms forbigående natur skaber et hurtigt skiftende magnetfelt, der inducerer en elektrisk strøm i hjernen4. I tilfælde af en enkelt TMS-stimulus aktiverer den inducerede strøm en række excitatoriske indgange til de pyramidale motorneuroner 5-7. Hvis styrken af de genererede excitatoriske input er tilstrækkelig, fremkalder den faldende aktivitet et kontralateralt muskulært respons kendt som det motorfremkaldte potentiale (MEP). MEP’ens latenstid afspejler den kortikomotoriske ledningstid8. Amplituden af MEP indekserer excitabiliteten af kortikospinale neuroner9. Den enkelte TMS-stimulus, der fremkalder MEP’en, kan også indledes med en konditioneringsstimulus10,11,12. Disse parrede pulsparadigmer kan bruges til at indeksere virkningerne af forskellige interneuronpuljer på kortikospinaludgangen. I tilfælde af SAI bruges den perifere elektriske konditioneringsstimulus til at undersøge virkningen af den afferente volley på motorens kortikale excitabilitet11,13,14,15. Den relative timing af TMS-stimulus og perifer elektrisk stimulering justerer virkningen af TMS-stimulus på motorcortex med ankomsten af de afferente fremskrivninger til motorcortex. For SAI i de distale muskler i overekstremiteterne går mediannervestimulus typisk forud for TMS-stimulus med 18-24 ms11,13,15,16. Samtidig øges SAI, da styrken af den afferente volley induceret af den perifere stimulus stiger13,17,18.

På trods af sin stærke tilknytning til de ydre egenskaber ved den afferente projektion til motorcortex er SAI et formbart fænomen, der er impliceret i mange motorstyringsprocesser. For eksempel reduceres SAI i opgaverelevante muskler før en forestående bevægelse 19,20,21, men opretholdes i tilstødende opgave-irrelevante motoriske repræsentationer19,20,22. Følsomheden over for opgaverelevans antages at afspejle en omgivende hæmningsmekanisme23, der sigter mod at reducere uønsket effektorrekruttering. For nylig blev det foreslået, at reduktionen i OR i den opgaverelevante effektor kan afspejle et bevægelsesrelateret gatingfænomen, der er designet til at undertrykke forventet sensorisk afferens21 og lette korrektioner under sensorimotorisk planlægning og udførelse24. Uanset den specifikke funktionelle rolle er SAI korreleret med reduktioner i manuel fingerfærdighed og behandlingseffektivitet25. Ændret SAI er også forbundet med en øget risiko for at falde hos ældre voksne 26 og kompromitteret sensorimotorisk funktion ved Parkinsons sygdom 26,27,28 og personer med fokal hånddystoni 29.

Klinisk og farmakologisk dokumentation indikerer, at de hæmmende veje, der medierer SAI, er følsomme over for central kolinerg modulation30. For eksempel reducerer administration af muskarin acetylcholinreceptorantagonist scopolamin SAI31. I modsætning hertil øger halveringstiden for acetylcholin via acetylcholinesterasehæmmere SAI32,33. I overensstemmelse med farmakologisk evidens er SAI følsom over for flere kognitive processer med central kolinerg involvering, herunder ophidselse 34, belønning35, tildeling af opmærksomhed 21,36,37 og hukommelse38,39,40. SAI ændres også i kliniske populationer med kognitive underskud forbundet med tab af kolinerge neuroner, såsom Alzheimers sygdom 41,42,43,44,45,46,47, Parkinsons sygdom (med mild kognitiv svækkelse)48,49,50 og mild kognitiv svækkelse 47,51,52. Differentialmodulationen af SAI af forskellige benzodiazepiner med differentielle affiniteter for forskellige γ-aminosmørsyre type A (GABAA) receptorunderenhedstyper antyder, at SAI-hæmmende veje adskiller sig fra veje, der medierer andre former for parret pulshæmning30. For eksempel nedsætter lorazepam SAI, men forbedrer korttids kortikal hæmning (SICI)53. Zolpidem reducerer SAI, men har ringe effekt på SICI53. Diazepam øger SICI, men har ringe indflydelse på SAI53. Reduktionen i SAI af disse positive allosteriske modulatorer af GABAA-receptorfunktion kombineret med observationen om, at GABA styrer frigivelsen af acetylcholin i hjernestammen og cortex54, har ført til hypotesen om, at GABA modulerer den kolinerge vej, der projicerer til den sensorimotoriske cortex for at påvirke SAI55.

For nylig er SAI blevet brugt til at undersøge interaktioner mellem de sensorimotoriske sløjfer, der indstiller proceduremæssige motorstyringsprocesser, og dem, der tilpasser proceduremæssige processer til eksplicitte top-down-mål og kognitive kontrolprocesser 21,36,37,38. Den centrale kolinerge involvering i SAI31 tyder på, at OR kan indeksere en udøvende indflydelse på proceduremæssig sensorimotorisk kontrol og læring. Det er vigtigt, at disse undersøgelser er begyndt at identificere de unikke virkninger af kognition på specifikke sensorimotoriske kredsløb ved at vurdere SAI ved hjælp af forskellige TMS-strømretninger. SAI-undersøgelser anvender typisk posterior-anterior (PA) induceret strøm, mens kun en håndfuld SAI-undersøgelser har anvendt anterior-posterior (AP) induceret strøm55. Brug af TMS til at inducere AP sammenlignet med PA-strøm under SAI-vurdering rekrutterer imidlertid forskellige sensorimotoriske kredsløb16,56. For eksempel ændres AP-følsomme, men ikke PA-følsomme, sensorimotoriske kredsløb ved cerebellær modulation37,56. Desuden moduleres AP-følsomme, men ikke PA-følsomme, sensorimotoriske kredsløb af opmærksomhedsbelastning36. Endelig kan opmærksomhed og cerebellære påvirkninger konvergere på de samme AP-følsomme sensorimotoriske kredsløb, hvilket fører til maladaptive ændringer i disse kredsløb37.

Fremskridt inden for TMS-teknologi giver yderligere fleksibilitet til at manipulere konfigurationen af TMS-stimulus, der anvendes under enkeltpuls, parret puls og gentagne applikationer57,58. Kontrollerbare pulsparameter TMS (cTMS) stimulatorer er nu kommercielt tilgængelige til forskningsbrug over hele verden, og disse giver fleksibel kontrol over pulsbredden og formen57. Den øgede fleksibilitet stammer fra styring af afladningsvarigheden af to uafhængige kondensatorer, der hver især er ansvarlige for en separat fase af TMS-stimulus. Den bifasiske eller monofasiske karakter af stimulus styres af den relative udledningsamplitude fra hver kondensator, en parameter kaldet M-forholdet. cTMS-undersøgelser har kombineret pulsbreddemanipulation med forskellige strømretninger for at demonstrere, at de faste pulsbredder, der anvendes af konventionelle TMS-stimulatorer (70-82 μs)59,60, sandsynligvis rekrutterer en blanding af funktionelt forskellige sensorimotoriske kredsløb under SAI 56. Derfor er cTMS et spændende værktøj til yderligere at udrede den funktionelle betydning af forskellige konvergerende sensorimotoriske sløjfer i sensorimotorisk ydeevne og læring.

Dette manuskript beskriver en unik SAI-tilgang til at studere sensorimotorisk integration, der integrerer perifer elektrisk stimulering med cTMS under sensorimotorisk adfærd. Denne tilgang forbedrer den typiske SAI-tilgang ved at vurdere effekten af afferente fremskrivninger på udvalgte interneuronpopulationer i motorcortexen, der styrer kortikospinalproduktionen under løbende sensorimotorisk adfærd. Selvom det er relativt nyt, giver cTMS en klar fordel ved at studere sensorimotorisk integration i typiske og kliniske populationer. Desuden kan den nuværende tilgang let tilpasses til brug med konventionelle TMS-stimulatorer og til at kvantificere andre former for afferent hæmning og facilitering, såsom langlatens afferent inhibition (LAI)13 eller kort-latency afferent facilitation (SAF)15.

Protocol

Følgende protokol kan anvendes på forskellige eksperimenter. De angivne oplysninger beskriver et eksperiment, hvor SAI bruges til at kvantificere sensorimotorisk integration under et fingerrespons på en gyldigt eller ugyldigt cued sonde. I denne protokol vurderes SAI uden en opgave, derefter samtidigt under cued sensorimotorisk opgave og derefter igen uden en opgave. cTMS-stimulatoren kan erstattes af enhver kommercielt tilgængelig konventionel TMS-stimulator. Imidlertid ville pulsbredden på den konventionelle TMS-s…

Representative Results

Figur 3 illustrerer eksempler på ubetingede og betingede MEP’er fra en enkelt deltager, der fremkaldes i FDI-musklen under den sensorimotoriske opgave ved hjælp af PA120- og AP30- (abonnement angiver pulsbredde) induceret strøm. Søjlediagrammerne i den midterste kolonne illustrerer de rå gennemsnitlige peak-to-peak MEP-amplituder for de ubetingede og betingede forsøg. Søjlediagrammerne til højre viser SAI- og MEP-startlatenstiden for PA120- og AP…

Discussion

SAI-metoden, der beskrives her, undersøger en delmængde af neurale veje, der spiller en rolle i sensorimotorisk ydeevne og læring. Vurdering af SAI, mens deltagerne udfører kontrollerede sensorimotoriske opgaver, er afgørende for at adskille de komplekse bidrag fra de mange sensorimotoriske sløjfer, der konvergerer på de motoriske kortikospinale neuroner for at forme motorudgangen i sunde og kliniske populationer. For eksempel er en lignende metode blevet anvendt til at identificere cerebellar indflydelse på proc…

Divulgations

The authors have nothing to disclose.

Acknowledgements

Forfatterne anerkender finansiering fra Natural Sciences and Engineering Research Council (NSERC), Canada Foundation for Innovation (CFI) og Ontario Research Fund (ORF) tildelt S.K.M.

Materials

Acquisition software (for EMG) AD Instruments, Colorado Springs, CO, USA PL3504/P LabChart Pro version 8
Alcohol prep pads Medline Canada Corporation, Mississauga, ON, Canada 211-MM-05507 Alliance Sterile Medium, Antiseptic Isopropyl Alcohol Pad (200 per box)
Amplifier (for EMG) AD Instruments, Colorado Springs, CO, USA FE234 Quad Bio Amp
Cotton round Cliganic, San Francisco, CA, USA ‎CL-BE-019-6PK Premium Cotton Rounds (6-pack, 90 per package)
cTMS coils Rogue Research, Montréal, QC, Canada COIL70F80301 70 mm Medium Inductance Figure-8 coil
cTMS coils Rogue Research, Montréal, QC, Canada COIL70F80301-IC 70 mm Medium Inductance Figure-8 coil (Inverted Current)
cTMS stimulator Rogue Research, Montréal, QC, Canada CTMSMU0101 Elevate cTMS stimulator
Data acquisition board (for EMG) AD Instruments, Colorado Springs, CO, USA PL3504 PowerLab 4/35
Digital to analog board National Instruments, Austin, TX, USA 782251-01 NI USB-6341, X Series DAQ Device with BNC Termination
Dispoable adhesive electrodes (for EMG) Covidien, Dublin, Ireland 31112496 Kendal 130 Foam Electrodes
Electrogel Electrodestore.com E9 Electro-Gel for Electro-Cap (16 oz jar)
Nuprep Weaver and Company, Aurora, CO, USA 10-30 Nuprep skin prep gel (3-pack of 4 oz tubes) 
Peripheral electrical stimulator Digitimer, Hertfordshire, UK DS7R  DS7R High Voltage Constant Current Stimulator
Reusable bar electrode Electrodestore.com DDA-30 Black Bar Electrode, Flat, Cathode Distal
Software (for behaviour and stimulator triggering) National Instruments, Austin, TX, USA 784503-35 Labview 2020
TMS stereotactic coil guidance system Rogue Research, Montréal, QC, Canada KITBSF0404 BrainSight Neuronavigation System
Transpore tape 3M, Saint Paul, MN, USA 50707387794571 Transpore Medical Tape (1 in x 10 yds)
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Keywords: Sensorimotor ControlMotor LearningSensory-motor IntegrationAfferent InhibitionTranscranial Magnetic StimulationControllable Pulse Parameter TMSMotor CortexMotor PerformanceSkill AcquisitionRehabilitationNeurological Disorders
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Graham, K. R., Hayes, K. D., Meehan, S. K. Combined Peripheral Nerve Stimulation and Controllable Pulse Parameter Transcranial Magnetic Stimulation to Probe Sensorimotor Control and Learning. J. Vis. Exp. (194), e65212, doi:10.3791/65212 (2023).
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