Divisive gain modulation of motoneurons by inhibition optimizes muscular control

Journal of Neuroscience

Volumn 35, Issue 8, 2015, Pages 3711-3723

  Vestergaard, Mikkel ^a   Berg, Rune W ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Control; Divisive; Gain; Inhibition; Motoneuron; Optimal

Indexed keywords

STRYCHNINE;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FEMALE; HYPERPOLARIZATION; IMMUNOHISTOCHEMISTRY; LIMB MOVEMENT; MALE; MEMBRANE POTENTIAL; MICROELECTRODE; MOTONEURON; MOTOR COORDINATION; MUSCLE STRENGTH; NERVE CONDUCTION; NERVE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SPIKE WAVE; STIMULUS RESPONSE; TURTLE; ACTION POTENTIAL; ANIMAL; HINDLIMB; INNERVATION; NERVE CELL INHIBITION; NEUROMUSCULAR SYNAPSE; NEUROPHYSIOLOGICAL RECRUITMENT; PHYSIOLOGY; SKELETAL MUSCLE; TOUCH;

ACTION POTENTIALS; ANIMALS; FEMALE; HINDLIMB; MALE; MEMBRANE POTENTIALS; MOTOR NEURONS; MUSCLE, SKELETAL; NEURAL INHIBITION; NEUROMUSCULAR JUNCTION; RECRUITMENT, NEUROPHYSIOLOGICAL; TOUCH; TURTLES;

EID: 84923343864     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3899-14.2015     Document Type: Article

References (64)

1. Alaburda A, Hounsgaard J (2003) Metabotropic modulation of motoneurons by scratch-like spinal network activity. J Neurosci 23:8625–8629. Medline.
2. Alaburda A, Russo R, MacAulay N, Hounsgaard J (2005) Periodic highconductance states in spinal neurons during scratch-like network activity in adult turtles. J Neurosci 25:6316–6321. CrossRef Medline.
3. Berg RW, Alaburda A, Hounsgaard J (2007) Balanced inhibition and excitation drive spike activity in spinal half-centers. Science 315:390–393. CrossRef Medline.
4. Berg RW, Ditlevsen S, Hounsgaard J (2008) Intense synaptic activity en-hances temporal resolution in spinal motoneurons. PLoS One 3:e3218. CrossRef Medline.
5. Berkowitz A, Stein PS (1994) Activity of descending propriospinal axons in the turtle hindlimb enlargement during two forms of fictive scratching: Broad tuning to regions of the body surface. J Neurosci 14:5089–5104. Medline.
6. Burke RE (1981) Motor units: Anatomy, physiology, and functional organization. In: Handbook of physiology: the nervous system (Brooks VB, Brookhart JM, eds), pp 345–422. Bethesda, MD: American Physiological Society.
7. Carandini M, Heeger DJ (2012) Normalization as a canonical neural computation. Nat Rev Neurosci 13:51–62. CrossRef Medline.
8. Chance FS, Abbott LF, Reyes AD (2002) Gain modulation from background synaptic input. Neuron 35:773–782. CrossRef Medline.
9. de Almeida AT, Kirkwood PA (2010) Multiple phases of excitation and inhibition in central respiratory drive potentials of thoracic motoneurones in the rat. J Physiol 588:2731–2744. CrossRef Medline.
10. Dideriksen JL, Negro F, Enoka RM, Farina D (2012) Motor unit recruitment strategies and muscle properties determine the influence of synaptic noise on force steadiness. J Neurophysiol 107:3357–3369. CrossRef Medline.
11. Enoka RM, Fuglevand AJ (2001) Motor unit physiology: Some unresolved issues. Muscle Nerve 24:4–17. CrossRef Medline.
12. Faisal AA, Selen LP, Wolpert DM (2008) Noise in the nervous system. Nat Rev Neurosci 9:292–303. CrossRef Medline.
13. Feinstein B, Lindegard B, Nyman E, Wohlfart G (1955) Morphologic studies of motor units in normal human muscles. Acta Anatomica 23:127–142. CrossRef Medline.
14. Field EC, Stein PS (1997) Spinal cord coordination of hindlimb movements in the turtle: Intralimb temporal relationships during scratching and swimming. J Neurophysiol 78:1394–1403. Medline.
15. Fuglevand AJ, Winter DA, Patla AE (1993) Models of recruitment and rate coding organization in motor-unit pools. J Neurophysiol 70:2470–2488. Medline.
16. Garnett RA, O’Donovan MJ, Stephens JA, Taylor A (1979) Motor unit organization of human medial gastrocnemius. J Physiol 287:33–43. CrossRef Medline.
17. Guimaraes AC, Herzog W, Hulliger M, Zhang YT, Day S (1994) EMG-force relationship of the cat soleus muscle studied with distributed and nonperiodic stimulation of ventral root filaments. J Exp Biol 186:75–93. Medline.
18. Guzulaitis R, Alaburda A, Hounsgaard J (2014) Dense distributed processing in a hindlimb scratch motor network. J Neurosci 34:10756–10764. CrossRef Medline.
19. Hansel D, van Vreeswijk C (2002) How noise contributes to contrast invariance of orientation tuning in cat visual cortex. J Neurosci 22:5118–5128. Medline.
20. Harris CM, Wolpert DM (1998) Signal-dependent noise determines motor planning. Nature 394:780–784. CrossRef Medline.
21. Hatze H (1979) A teleological explanation of Weber’s law and the motor unit size law. Bulletin of Mathematical Biology 41:407–425. CrossRef Medline.
22. Heckman CJ, Mottram C, Quinlan K, Theiss R, Schuster J (2009) Motoneuron excitability: The importance of neuromodulatory inputs. Clin Neurophysiol 120:2040–2054. CrossRef Medline.
23. Henneman E, Mendell L (1981) Functional organization of motoneuron pool and its inputs. In: Handbook of physiology: The nervous system (Brooks VB, Brookhart JM, eds), pp 423–458. Bethesda, MD: American Physiological Society.
24. Ho N, Destexhe A (2000) Synaptic background activity enhances the responsiveness of neocortical pyramidal neurons. J Neurophysiol 84:1488–1496. Medline.
25. Hounsgaard J, Kiehn O (1989) Serotonin-induced bistability of turtle motoneurones caused by a nifedipine-sensitive calcium plateau potential. J Physiol 414:265–282. Medline.
26. Hultborn H, Lindström S, Wigström H (1979) On the function of recurrent inhibition in the spinal cord. Exp Brain Res 37:399–403. Medline.
27. Hultborn H, Denton ME, Wienecke J, Nielsen JB (2003) Variable amplification of synaptic input to cat spinal motoneurones by dendritic persistent inward current. J Physiol 552:945–952. CrossRef Medline.
28. Jahn P, Berg RW, Hounsgaard J, Ditlevsen S (2011) Motoneuron membrane potentials follow a time inhomogeneous jump diffusion process. J Comput Neurosci 31:563–579. CrossRef Medline.
29. Johnson MD, Heckman CJ (2014) Gain control mechanisms in spinal motoneurons. Front Neural Circuits 8:81. CrossRef Medline.
30. Johnson MD, Hyngstrom AS, Manuel M, Heckman CJ (2012) Push–pull control of motor output. J Neurosci 32:4592–4599. CrossRef Medline.
31. Jones KE, Hamilton AF, Wolpert DM (2002) Sources of signal-dependent noise during isometric force production. J Neurophysiol 88:1533–1544. Medline.
32. Keifer J, Stein PS (1983) In vitro motor program for the rostral scratch reflex generated by the turtle spinal cord. Brain Res 266:148–151. CrossRef Medline.
33. Kernell D, Hultborn H (1990) Synaptic effects on recruitment gain: a mechanism of importance for the input-output relations of motoneurone pools? Brain Res 507:176–179. CrossRef Medline.
34. Kolind J, Hounsgaard J, Berg RW (2012) Opposing effects of intrinsic conductance and correlated synaptic input on Vm-fluctuations during network activity. Front Comput Neurosci 6:40. CrossRef Medline.
35. Mendell LM (2005) The size principle: A rule describing the recruitment of motoneurons. J Neurophysiol 93:3024–3026. CrossRef Medline.
36. Miles GB, Hartley R, Todd AJ, Brownstone RM (2007) Spinal cholinergic interneurons regulate the excitability of motoneurons during locomotion. Proc Natl Acad Sci U S A 104:2448–2453. CrossRef Medline.
37. Miller KD, Troyer TW (2002) Neural noise can explain expansive, powerlaw nonlinearities in neural response functions. J Neurophysiol 87:653–659. Medline.
38. Milner-Brown HS, Stein RB, Yemm R (1973) The orderly recruitment of human motor units during voluntary isometric contractions. J Physiol 230:359–370. CrossRef Medline.
39. Mitchell SJ, Silver RA (2003) Shunting inhibition modulates neuronal gain during synaptic excitation. Neuron 38:433–445. CrossRef Medline.
40. Mortin LI, Keifer J, Stein PS (1985) Three forms of the scratch reflex in the spinal turtle: Movement analyses. J Neurophysiol 53:1501–1516. Medline.
41. Murphy BK, Miller KD (2003) Multiplicative gain changes are induced by excitation or inhibition alone. J Neurosci 23:10040–10051. Medline.
42. Noga BR, Kriellaars DJ, Brownstone RM, Jordan LM (2003) Mechanism for activation of locomotor centers in the spinal cord by stimulation of the mesencephalic locomotor region. J Neurophysiol 90:1464–1478. CrossRef Medline.
43. ParkerD (2003) Activity-dependent feedforward inhibition modulates synaptic transmission in a spinal locomotor network. J Neurosci 23:11085–11093. Medline.
44. Parkis MA, Dong X, Feldman JL, Funk GD (1999) Concurrent inhibition and excitation of phrenic motoneurons during inspiration: Phase-specific control of excitability. J Neurosci 19:2368–2380. Medline.
45. Perrier JF, Hounsgaard J (2000) Development and regulation of response properties in spinal cord motoneurons. Brain Res Bull 53:529–535. CrossRef Medline.
46. Petersen PC, Vestergaard M, Jensen KH, Berg RW (2014) Premotor spinal network with balanced excitation and inhibition during motor patterns has high resilience to structural division. J Neurosci 34:2774–2784. CrossRef Medline.
47. Polack PO, Friedman J, Golshani P (2013) Cellular mechanisms of brain state-dependent gain modulation in visual cortex. Nat Neurosci 16:1331–1339. CrossRef Medline.
48. Powers RK, Elbasiouny SM, Rymer WZ, Heckman CJ (2012) Contribution of intrinsic properties and synaptic inputs to motoneuron discharge patterns: A simulation study. J Neurophysiol 107:808–823. CrossRef Medline.
49. Rabinowitz NC, Willmore BD, Schnupp JW, King AJ (2011) Contrast gain control in auditory cortex. Neuron 70:1178–1191. CrossRef Medline.
50. Rekling JC, Funk GD, Bayliss DA, Dong XW, Feldman JL (2000) Synaptic control of motoneuronal excitability. Physiol Rev 80:767–852. Medline.
51. Ruigrok TJ, Crowe A, ten Donkelaar HJ (1984) Morphology of lumbar motoneurons innervating hindlimb muscles in the turtle Pseudemys scrìpta elegans: An intracellular horseradish peroxidase study. J Comp Neurol 230:413–425. CrossRef Medline.
52. Saywell SA, Feldman JL (2004) Dynamic interactions of excitatory and inhibitory inputs in hypoglossal motoneurones: Respiratory phasing and modulation by PKA. J Physiol 554:879–889. CrossRef Medline.
53. Senn W, Wyler K, Clamann HP, Kleinle J, Lüscher, HR, Müller L (1997) Size principle and information theory. Biol Cybern 76:11–22. CrossRef Medline.
54. Silver RA (2010) Neuronal arithmetic. Nat Rev Neurosci 11:474–489. CrossRef Medline.
55. Stein PS (2005) Neuronal control of turtle hindlimb motor rhythms. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 191:213–229. CrossRef Medline.
56. Stein RB, Gossen ER, Jones KE (2005) Neuronal variability: Noise or part of the signal? Nature Rev Neurosci 6:389–397. Medline.
57. Takei T, Seki K (2013) Spinal premotor interneurons mediate dynamic and static motor commands for precision grip in monkeys. J Neurosci 33: 8850–8860. CrossRef Medline.
58. Todorov E (2004) Optimality principles in sensorimotor control. Nat Neurosci 7:907–915. CrossRef Medline.
59. Walløe S, Nissen UV, Berg RW, Hounsgaard J, Pakkenberg B (2011) Stereological estimate of the total number of neurons in spinal segment D9 of the red-eared turtle. J Neurosci 31:2431–2435. CrossRef Medline.
60. Watanabe RN, Magalha˜es FH, Elias LA, Chaud VM, Mello EM, Kohn AF (2013) Influences of premotoneuronal command statistics on the scaling of motor output variability during isometric plantar flexion. J Neurophysiol 110:2592–2606. CrossRef Medline.
61. Wei K, Glaser JI, Deng L, Thompson CK, Stevenson IH, Wang Q, Hornby TG, Heckman CJ, Kording KP (2014) Serotonin affects movement gain control in the spinal cord. J Neurosci 34:12690–12700. CrossRef Medline.
62. Wilson NR, Runyan CA, Wang FL, Sur M (2012) Division and subtraction by distinct cortical inhibitory networks in vivo. Nature 488:343–348. CrossRef Medline.
63. Windhorst U (1996) On the role of recurrent inhibitory feedback in motor control. Prog Neurobiol 49:517–587. CrossRef Medline.
64. Wu G, Perlmutter SI (2013) Sensitivity of spinal neurons to GABA and glycine during voluntary movement in behaving monkeys. J Neurophysiol 109:193–201. CrossRef Medline.