Reorganization of Motor Cortex by Vagus Nerve Stimulation Requires Cholinergic Innervation

Brain Stimulation

Volumn 9, Issue 2, 2016, Pages 174-181

  Hulsey, Daniel R ^a   Hays, Seth A ^a,b   Khodaparast, Navid ^a   Ruiz, Andrea ^a   Das, Priyanka ^b   Rennaker, Robert L ^a,b   Kilgard, Michael P ^a  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

^b The University of Texas at Dallas   (United States)

Author keywords

Acetylcholine; Cortical plasticity; Cortical reorganization; Immunotoxin; Motor cortex; Motor training; Nucleus basalis; Vagal nerve stimulation; Vagus nerve stimulation

Indexed keywords

IMMUNOTOXIN; IMMUNOTOXIN 192 IGG SAPORIN; UNCLASSIFIED DRUG; 192 IGG-SAPORIN; MONOCLONAL ANTIBODY; RIBOSOME INACTIVATING PROTEIN 1;

ADULT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; BRAIN DAMAGE; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; EXPERIMENTAL BEHAVIORAL TEST; FEMALE; FORELIMB; INJECTION; LEVER PRESSING TASK; MOTOR CORTEX; MOTOR PERFORMANCE; MOVEMENT (PHYSIOLOGY); NERVE CELL PLASTICITY; NONHUMAN; PARASYMPATHETIC INNERVATION; PRIORITY JOURNAL; RAT; TASK PERFORMANCE; VAGUS NERVE STIMULATION; ANIMAL; CYTOLOGY; DRUG EFFECTS; MEYNERT BASAL NUCLEUS; PATHOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; ANTIBODIES, MONOCLONAL; BASAL NUCLEUS OF MEYNERT; CHOLINERGIC NEURONS; FEMALE; MOTOR CORTEX; MOVEMENT; NEURONAL PLASTICITY; RATS; RATS, SPRAGUE-DAWLEY; RIBOSOME INACTIVATING PROTEINS, TYPE 1; VAGUS NERVE STIMULATION;

EID: 84961135629     PISSN: 1935861X     EISSN: 18764754     Source Type: Journal    
DOI: 10.1016/j.brs.2015.12.007     Document Type: Article

References (64)

1. S.A. Hays, R.L. Rennaker II, and M.P. Kilgard Targeting plasticity with vagus nerve stimulation to treat neurological disease Prog Brain Res 207 2013 275 299
2. N.D. Engineer, J.R. Riley, J.D. Seale, W.A. Vrana, J.A. Shetake, S.P. Sudanagunta, and et al. Reversing pathological neural activity using targeted plasticity Nature 470 2011 101 104
3. J.A. Shetake, N.D. Engineer, W.A. Vrana, J.T. Wolf, and M.P. Kilgard Pairing tone trains with vagus nerve stimulation induces temporal plasticity in auditory cortex Exp Neurol 233 2011 342 349
4. C.T. Engineer, N.D. Engineer, J.R. Riley, J.D. Seale, and M.P. Kilgard Pairing speech sounds with vagus nerve stimulation drives stimulus-specific cortical plasticity Brain Stimul 8 2015 637 644
5. B.A. Porter, N. Khodaparast, T. Fayyaz, R.J. Cheung, S.S. Ahmed, W.A. Vrana, and et al. Repeatedly pairing vagus nerve stimulation with a movement reorganizes primary motor cortex Cereb Cortex 22 2011 2365 2374
6. D. De Ridder, S. Vanneste, N.D. Engineer, and M.P. Kilgard Safety and efficacy of vagus nerve stimulation paired with tones for the treatment of tinnitus: a case series Neuromodulation 17 2014 170 179
7. D. De Ridder, M. Kilgard, N. Engineer, and S. Vanneste Placebo-controlled vagus nerve stimulation paired with tones in a patient with refractory tinnitus: a case report Otol Neurotol 36 2015 575 580
8. N. Khodaparast, S.A. Hays, A.M. Sloan, D.R. Hulsey, A. Ruiz, M. Pantoja, and et al. Vagus nerve stimulation during rehabilitative training improves forelimb strength following ischemic stroke Neurobiol Dis 60 2013 80 88
9. N. Khodaparast, S.A. Hays, A.M. Sloan, T. Fayyaz, D.R. Hulsey, R.L. Rennaker II, and et al. Vagus nerve stimulation delivered during motor rehabilitation improves recovery in a rat model of stroke Neurorehabil Neural Repair 28 2014 698 706
10. S.A. Hays, N. Khodaparast, A. Ruiz, A.M. Sloan, D.R. Hulsey, R.L. Rennaker, and et al. The timing and amount of vagus nerve stimulation during rehabilitative training affect post-stroke recovery of forelimb strength Neuroreport 25 9 2014 676 682
11. S.A. Hays, N. Khodaparast, D.R. Hulsey, A. Ruiz, A.M. Sloan, R.L. Rennaker II, and et al. Vagus nerve stimulation during rehabilitative training improves functional recovery after intracerebral hemorrhage Stroke 45 2014 3097 3100
12. D. Pruitt, A. Schmid, L. Kim, C. Abe, J. Trieu, C. Choua, and et al. Vagus nerve stimulation delivered with motor training enhances recovery of function after traumatic brain injury J Neurotrauma 32 2015 1 9
13. Microtransponder Paired vagus nerve stimulation (VNS) with rehabilitation for upper limb function improvement after stroke ClinicalTrials gov 2014 National Library of Medicine (US) Bethesda, MD NCT01669161 https://clinicaltrials.gov/ct2/show/NCT01669161
14. Microtransponder VNS during rehabilitation for improved upper limb motor function after stroke ClinicalTrials gov 2014 National Library of Medicine (US) Bethesda, MD NCT02243020 https://clinicaltrials.gov/ct2/show/study/NCT02243020
15. G.L. Morris, and W.M. Mueller Long-term treatment with vagus nerve stimulation in patients with refractory epilepsy Neurology 53 1999 1731 1735
16. M.S. George, H.A. Sackeim, A.J. Rush, L.B. Marangell, Z. Nahas, M.M. Husain, and et al. Vagus nerve stimulation: a new tool for brain research and therapy Biol Psychiatry 47 2000 287 295
17. H.A. Sackeim, A.J. Rush, M.S. George, L.B. Marangell, M.M. Husain, Z. Nahas, and et al. Vagus nerve stimulation (VNS™) for treatment-resistant depression: efficacy, side effects, and predictors of outcome Neuropsychopharmacology 25 2001 713 728
18. D.J. Englot, Chang E.F., and K.I. Auguste Vagus nerve stimulation for epilepsy: a meta-analysis of efficacy and predictors of response: a review J Neurosurg 115 2011 1248 1255
19. D.A. Groves, and V.J. Brown Vagal nerve stimulation: a review of its applications and potential mechanisms that mediate its clinical effects Neurosci Biobehav Rev 29 2005 493 500
20. L. Detari, G. Juhasz, and T. Kukorelli Effect of stimulation of vagal and radial nerves on neuronal activity in the basal forebrain area of anaesthetized cats Acta Physiol Hung 61 1983 147 154
21. D.A. Groves, E.M. Bowman, and V.J. Brown Recordings from the rat locus coeruleus during acute vagal nerve stimulation in the anaesthetised rat Neurosci Lett 379 2005 174 179
22. S. Manta, Dong J., G. Debonnel, and P. Blier Enhancement of the function of rat serotonin and norepinephrine neurons by sustained vagus nerve stimulation J Psychiatry Neurosci 34 2009 272 280
23. D. Hassert, T. Miyashita, and C. Williams The effects of peripheral vagal nerve stimulation at a memory-modulating intensity on norepinephrine output in the basolateral amygdala Behav Neurosci 118 2004 79 88
24. R.W. Roosevelt, D.C. Smith, R.W. Clough, R.A. Jensen, and R.A. Browning Increased extracellular concentrations of norepinephrine in cortex and hippocampus following vagus nerve stimulation in the rat Brain Res 1119 2006 124 132
25. P. Follesa, F. Biggio, G. Gorini, S. Caria, G. Talani, L. Dazzi, and et al. Vagus nerve stimulation increases norepinephrine concentration and the gene expression of BDNF and bFGF in the rat brain Brain Res 1179 2007 28 34
26. A.M. Landau, S. Dyve, S. Jakobsen, A.K. Alstrup, A. Gjedde, and D.J. Doudet Acute vagal nerve stimulation lowers α2 adrenoceptor availability: possible mechanism of therapeutic action Brain Stimul 8 2015 702 707
27. S.E. Krahl, K.B. Clark, D.C. Smith, and R.A. Browning Locus coeruleus lesions suppress the seizure-attenuating effects of vagus nerve stimulation Epilepsia 39 1998 709 714
28. A. Grimonprez, R. Raedt, J. Portelli, I. Dauwe, L.E. Larsen, C. Bouckaert, and et al. The antidepressant-like effect of vagus nerve stimulation is mediated through the locus coeruleus J Psychiatr Res 68 2015 1 7
29. J. Nichols, A. Nichols, S. Smirnakis, N. Engineer, M. Kilgard, and M. Atzori Vagus nerve stimulation modulates cortical synchrony and excitability through the activation of muscarinic receptors Neuroscience 189 2011 207 214
30. Gu Q. Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity Neuroscience 111 2002 815 835
31. M.F. Bear, and W. Singer Modulation of visual cortical plasticity by acetylcholine and noradrenaline Nature 320 1986 172 176
32. G.H. Seol, J. Ziburkus, Huang S.Y., Song L., I.T. Kim, K. Takamiya, and et al. Neuromodulators control the polarity of spike-timing-dependent synaptic plasticity Neuron 55 2007 919 929
33. S.A. Hays, N. Khodaparast, A.M. Sloan, T. Fayyaz, D.R. Hulsey, A.D. Ruiz, and et al. The bradykinesia assessment task: an automated method to measure forelimb speed in rodents J Neurosci Methods 214 2013 52 61
34. J.M. Conner, A.A. Chiba, and M.H. Tuszynski The basal forebrain cholinergic system is essential for cortical plasticity and functional recovery following brain injury Neuron 46 2005 173 179
35. D. Ramanathan, M.H. Tuszynski, and J.M. Conner The basal forebrain cholinergic system is required specifically for behaviorally mediated cortical map plasticity J Neurosci 29 2009 5992 6000
36. J. Conner, M. Kulczycki, and M. Tuszynski Unique contributions of distinct cholinergic projections to motor cortical plasticity and learning Cereb Cortex 20 2010 2739 2748
37. J.A. Kleim, R. Bruneau, K. Calder, D. Pocock, P.M. VandenBerg, E. MacDonald, and et al. Functional organization of adult motor cortex is dependent upon continued protein synthesis Neuron 40 2003 167 176
38. E. Neafsey, and C. Sievert A second forelimb motor area exists in rat frontal cortex Brain Res 232 1982 151 156
39. E. Neafsey, E. Bold, G. Haas, K. Hurley-Gius, G. Quirk, C. Sievert, and et al. The organization of the rat motor cortex: a microstimulation mapping study Brain Res 396 1986 77 96
40. Y. Gioanni, and M. Lamarche A reappraisal of rat motor cortex organization by intracortical microstimulation Brain Res 344 1985 49 61
41. P.L. Di Patre, C.W. Mathes, and L.L. Butcher Differential visualization of cholinesterasic neuronal somata and fibers by use of modifications of acetylcholinesterase pharmacohistochemistry J Histochem Cytochem 41 1993 129 135
42. C. Geula, and M.M. Mesulam Systematic regional variations in the loss of cortical cholinergic fibers in Alzheimer's disease Cereb Cortex 6 1996 165 177
43. J.M. Conner, M.A. Darracq, J. Roberts, and M.H. Tuszynski Nontropic actions of neurotrophins: subcortical nerve growth factor gene delivery reverses age-related degeneration of primate cortical cholinergic innervation PNAS 98 2001 1941 1946
44. J. Berger-Sweeney, S. Heckers, M.M. Mesulam, R.G. Wiley, D.A. Lappi, and M. Sharma Differential effects on spatial navigation of immunotoxin-induced cholinergic lesions of the medial septal area and nucleus basalis magnocellularis J Neurosci 14 1994 4507 4519
45. A.A. Chiba, D.J. Bucci, P.C. Holland, and M. Gallagher Basal forebrain cholinergic lesions disrupt increments but not decrements in conditioned stimulus processing J Neurosci 15 1995 7315 7322
46. J.J. Waite, M.L. Wardlow, Chen A.C., D.A. Lappi, R.G. Wiley, and L.J. Thal Time course of cholinergic and monoaminergic changes in rat brain after immunolesioning with 192 IgG-saporin Neurosci Lett 169 1994 154 158
47. J.M. Conner, A. Culberson, C. Packowski, A.A. Chiba, and M.H. Tuszynski Lesions of the basal forebrain cholinergic system impair task acquisition and abolish cortical plasticity associated with motor skill learning Neuron 38 2003 819 829
48. J.A. Kleim, S. Barbay, and R.J. Nudo Functional reorganization of the rat motor cortex following motor skill learning J Neurophysiol 80 1998 3321 3325
49. J.A. Kleim, N.R. Cooper, and P.M. VandenBerg Exercise induces angiogenesis but does not alter movement representations within rat motor cortex Brain Res 934 2002 1 6
50. P.M. VandenBerg, T.M. Hogg, J.A. Kleim, and I.Q. Whishaw Long-Evans rats have a larger cortical topographic representation of movement than Fischer-344 rats: a microstimulation study of motor cortex in naïve and skilled reaching-trained rats Brain Res Bull 59 2002 197 203
51. K. Molina-Luna, B. Hertler, M.M. Buitrago, and A.R. Luft Motor learning transiently changes cortical somatotopy Neuroimage 40 2008 1748 1754
52. A. Reed, J. Riley, R. Carraway, A. Carrasco, C. Perez, V. Jakkamsetti, and et al. Cortical map plasticity improves learning but is not necessary for improved performance Neuron 70 2011 121 131
53. M.P. Kilgard Harnessing plasticity to understand learning and treat disease Trends Neurosci 35 2012 715 722
54. R. Raedt, R. Clinckers, L. Mollet, K. Vonck, R. El Tahry, T. Wyckhuys, and et al. Increased hippocampal noradrenaline is a biomarker for efficacy of vagus nerve stimulation in a limbic seizure model J Neurochem 117 2011 461 469
55. D.V. Buonomano, and M.M. Merzenich Cortical plasticity: from synapses to maps Annu Rev Neurosci 21 1998 149 186
56. M.S. Rioult-Pedotti, D. Friedman, G. Hess, and J.P. Donoghue Strengthening of horizontal cortical connections following skill learning Nat Neurosci 1 1998 230 234
57. M. Rioult-Pedotti, D. Friedman, and J.P. Donoghue Learning-induced LTP in neocortex Science 290 2000 533 536
58. Zuo Y., D.C. Smith, and R.A. Jensen Vagus nerve stimulation potentiates hippocampal LTP in freely-moving rats Physiol Behav 90 2007 583 589
59. Shen H., Y. Fuchino, D. Miyamoto, H. Nomura, and N. Matsuki Vagus nerve stimulation enhances perforant path-CA3 synaptic transmission via the activation of β-adrenergic receptors and the locus coeruleus Int J Neuropsychopharmacol 15 2012 523 530
60. H. Ura, Y. Sugaya, H. Ohata, I. Takumi, K. Sadamoto, T. Shibasaki, and et al. Vagus nerve stimulation induced long-lasting enhancement of synaptic transmission and decreased granule cell discharge in the hippocampal dentate gyrus of urethane-anesthetized rats Brain Res 1492 2013 63 71
61. E.C. Burgard, and J.M. Sarvey Muscarinic receptor activation facilitates the induction of long-term potentiation (LTP) in the rat dentate gyrus Neurosci Lett 116 1990 34 39
62. T. Shinoe, M. Matsui, M.M. Taketo, and T. Manabe Modulation of synaptic plasticity by physiological activation of M1 muscarinic acetylcholine receptors in the mouse hippocampus J Neurosci 25 2005 11194 11200
63. Microtransponder Proof-of-concept study assessing VNS paired with tones for tinnitus ClinicalTrials gov 2010 National Library of Medicine (US) Bethesda, MD NCT01253616 http://clinicaltrials.gov/ct2/show/NCT01253616
64. Microtransponder Vagus nerve stimulation (VNS) paired with tones for tinnitus ClinicalTrials gov 2013 National Library of Medicine (US) Bethesda, MD NCT01962558 http://clinicaltrials.gov/ct2/show/NCT01962558