Serotonin 1A receptors alter expression of movement representations

Journal of Neuroscience

Volumn 33, Issue 11, 2013, Pages 4988-4999

  Scullion, Kathleen ^a,b   Boychuk, Jeffery A ^a   Yamakawa, Glenn R ^a,c   Rodych, Justin T G ^a,c   Nakanishi, Stan T ^b   Seto, Angela ^a,c   Smith, Victoria M ^a,c   McCarthy, Ryan W ^a,b   Whelan, Patrick J ^a,b   Antle, Michael C ^a,b,c   Pittman, Quentin J ^a,b   Teskey, G Campbell ^a,b,c  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

5, 7 DIHYDROXYTRYPTAMINE; N TERT BUTYL 3 [4 (2 METHOXYPHENYL) 1 PIPERAZINYL] 2 PHENYLPROPIONAMIDE; SEROTONIN 1A RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN CORTEX; CELL COUNT; CONTROLLED STUDY; DORSAL RAPHE NUCLEUS; ELECTROPHYSIOLOGY; ELECTROSTIMULATION; EXCITABILITY; FORELIMB; IMMUNOHISTOCHEMISTRY; MALE; MEDIAN RAPHE NUCLEUS; MOVEMENT (PHYSIOLOGY); NERVE CELL EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SPINAL CORD; STIMULATION;

5,7-DIHYDROXYTRYPTAMINE; 8-HYDROXY-2-(DI-N-PROPYLAMINO)TETRALIN; ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; BRAIN MAPPING; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; FORELIMB; H-REFLEX; MALE; MICE; MICE, KNOCKOUT; MICROINJECTIONS; MOTOR CORTEX; MOVEMENT; NEURONS; PATCH-CLAMP TECHNIQUES; PIPERAZINES; PSYCHOMOTOR PERFORMANCE; RAPHE NUCLEI; RATS; RATS, LONG-EVANS; RECEPTOR, SEROTONIN, 5-HT1A; SEROTONIN; SEROTONIN AGENTS; SPINAL CORD; TRYPTOPHAN HYDROXYLASE;

EID: 84874858632     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4241-12.2013     Document Type: Article

References (74)

1. Bandrowski AE, Huguenard JR, Prince DA (2003) Baseline glutamate levels affect group I and II mGluRs in layer V pyramidal neurons of rat sensorimotor cortex. J Neurophysiol 89:1308-1316. Medline
2. Barnes NM, Sharp T (1999) A review of central 5-HT receptors and their function. Neuropharmacology 38:1083-1152. CrossRef Medline
3. Bolay H, Dalkara T (1998) Mechanisms of motor dysfunction after transient MCA occlusion: persistent transmission failure in cortical synapses is a major determinant. Stroke 29:1988-1993; discussion 1994. CrossRef Medline
4. Bowker RM, Westlund KN, Sullivan MC, Wilber JF, Coulter JD (1983) Descending serotonergic, peptidergic and cholinergic pathways from the raphe nuclei: a multiple transmitter complex. Brain Res 288:33-48. CrossRef Medline
5. Boychuk JA, Adkins DL, Kleim JA (2011) Distributed versus focal cortical stimulation to enhance motor function and motor map plasticity in a rodent model of ischemia. Neurorehabil Neural Repair 25:88-97. CrossRef Medline
6. Brill J, Huguenard JR (2010) Enhanced infragranular and supragranular synaptic input onto layer 5 pyramidal neurons in a rat model of cortical dysplasia. Cereb Cortex 20:2926-2938. CrossRef Medline
7. Brown AR, Hu B, Antle MC, Teskey GC (2009) Neocortical movement representations are reduced and reorganized following bilateral intrastriatal 6-hydroxydopamine infusion and dopamine type-2 receptor antagonism. Exp Neurol 220:162-170. CrossRef Medline
8. Brown AR, Antle MC, Hu B, Teskey GC (2011) High frequency stimulation of the subthalamic nucleus acutely rescues motor deficits and neocortical movement representations following 6-hydroxydopamine administration in rats. Exp Neurol 231:82-90. CrossRef Medline
9. Cazalets JR, Sqalli-Houssaini Y, Clarac F (1992) Activation of the central pattern generators for locomotion by serotonin and excitatory amino acids in neonatal rat. J Physiol 455:187-204. Medline
10. Conner JM, Culberson A, Packowski C, Chiba AA, Tuszynski MH (2003) Lesions of the basal forebrain cholinergic system impair task acquisition and abolish cortical plasticity associated with motor skill learning. Neuron 38:819-829. CrossRef Medline
11. Conner JM, Kulczycki M, Tuszynski MH (2010) Unique contributions of distinct cholinergic projections to motor cortical plasticity and learning. Cereb Cortex 20:2739-2748. CrossRef Medline
12. Cowley KC, Schmidt BJ (1997) Regional distribution of the locomotor pattern-generating network in the neonatal rat spinal cord. J Neurophysiol 77:247-259. Medline
13. Croul S, Radzievsky A, Sverstiuk A, Murray M (1998) NK1, NMDA, 5HT1a, and 5HT2 receptor binding sites in the rat lumbar spinal cord: modulation following sciatic nerve crush. Exp Neurol 154:66-79. CrossRef Medline
14. Daval G, Verg é D, Basbaum AI, Bourgoin S, Hamon M (1987) Autoradiographic evidence of serotonin 1 binding sites on primary afferent fibres in the dorsal horn of the rat spinal cord. Neurosci Lett 16: 83:71-76. CrossRef
15. Dringenberg HC, Hargreaves EL, Baker GB, Cooley RK, Vanderwolf CH (1995) p-Chlorophenylalanine-induced serotonin depletion: reduction in exploratory locomotion but no obvious sensory-motor deficits. Behav Brain Res 68:229-237. CrossRef Medline
16. Elliott P, Wallis DI (1992) Serotonin and L-norepinephrine as mediators of altered excitability in neonatal rat motoneurons studied in vitro. Neuroscience 47:533-544. CrossRef Medline
17. Ferrier D (1873) Experimental researches in cerebral physiology and pathology. West Riding Lunatic Asylum Medical Reports 3:152-155.
18. Fink KB, Göthert M (2007) 5-HT receptor regulation of neurotransmitter release. Pharmacol Rev 59:360-417. CrossRef Medline
19. Flynn C, Young NA, Teskey GC (2010) Seizures, but not lowered seizure thresholds, results in larger neocortical motor maps and concomitant disruptions in skilled motor behaviour. Behav Brain Res 214:60-65. CrossRef Medline
20. Fritsch G, Hitzig E (1870) Ueber die elektrishe Erregarkeit des Qrosshirns. In: The cerebral cortex (Von BG, ed), pp 73-96. Springfield, IL: Thomas.
21. Galic MA, Riazi K, Heida JG, Mouihate A, Fournier NM, Spencer SJ, Kalynchuk LE, Teskey GC, Pittman QJ (2008) Neonatal inflammation increases seizure susceptibility in adult rats. J Neurosci 28:6904-6913. CrossRef Medline
22. Gharbawie OA, Whishaw IQ (2003) Cholinergic and serotonergic neocortical projection lesions given singly or in combination cause only mild impairments on tests of skilled movement in rats: evaluation of a model of dementia. Brain Res 970:97-109. CrossRef Medline
23. Gharbawie OA, Gonzalez CL, Williams PT, Kleim JA, Whishaw IQ (2005) Middle cerebral artery (MCA) stroke produces dysfunction in adjacent motor cortex as detected by intracortical microstimulation in rats. Neuroscience 130:601-610. CrossRef Medline
24. Graziano MS, Taylor CS, Moore T, Cooke DF (2002) The cortical control of movement revisited. Neuron 36:349-362. CrossRef Medline
25. Hall FS, Devries AC, Fong GW, Huang S, Pert A (1999) Effects of 5,7-dihydroxytryptamine depletion of tissue serotonin levels on extracellular serotonin in the striatum assessed with in vivo microdialysis: relationship to behavior. Synapse 33:16-25. CrossRef Medline
26. Hedlund PB, Sutcliffe JG (2004) Functional, molecular and pharmacological advances in 5-HT7 receptor research. Trends Pharmacol Sci 25:481-486. CrossRef Medline
27. Hedo G, Ajubita M, Lopez-Garcia JA (2002) Role of serotonin 1A receptors on the modulation of rat spinal mono-synaptic reflexes in vitro. Neurosci Lett 334:41-44. CrossRef Medline
28. Henderson AK, Galic MA, Fouad K, Dyck RH, Pittman QJ, Teskey GC (2011) Larger cortical motor maps after seizures. Eur J Neurosci 34: 615-621. CrossRef Medline
29. Henderson AK, Pittman QJ, Teskey GC (2012) High frequency stimulation alters motor maps, impairs skilled reaching performance and is accompanied by an upregulation of specific GABA, glutamate and NMDA receptor subunits. Neuroscience 215:98-113. CrossRef Medline
30. Henry LC, Goertzen CD, Lee A, Teskey GC (2008) Repeated seizures lead to altered skilled behaviour and are associated with more highly efficacious excitatory synapses. Eur J Neurosci 27:2165-2176. CrossRef Medline
31. Hess G, Donoghue JP (1994) Long-term potentiation of horizontal connections provides a mechanism to reorganize cortical motor maps. J Neurophysiol 71:2543-2547. Medline
32. Ho SM, Waite PM (2002) Effects of different anesthetics on the paired-pulse depression of the H-reflex in adult rat. Exp Neurol 177:494-503. CrossRef Medline
33. Hochman S, Schmidt BJ (1998) Whole cell recordings of lumbar motoneurons during locomotor-like activity in the in-vitro neonatal rat spinal cord. J Neurophysiol 79:743-752. Medline
34. Honda M, Imaida K, Tanabe M, Ono H (2004) Endogenously released 5-hydroxytryptamine depresses the spinal monosynaptic reflex via 5-HT1D receptors. Eur J Pharmacol 503:55-61. CrossRef Medline
35. Horn T, Bauce L, Landgraf R, Pittman QJ (1995) Microdialysis with high NaCl causes central release of amino acids and dopamine. J Neurochem 64:1632-1644. Medline
36. Hosoido T, Motoyama S, Goto M, Mori F, Tajima T, Hirata H, Wada N (2009) Characteristics of H-and M-waves recorded from rat forelimbs. Neurosci Lett 450:239-241. CrossRef Medline
37. Jackson DA, White SR (1990) Receptor subtypes mediating facilitation by serotonin of excitability of spinal motoneurons. Neuropharmacology 29: 787-797. CrossRef Medline
38. Jankowska E, Padel Y, Tanaka R (1975) The mode of activation of pyramidal tract cells by intracortical stimuli. J Physiol 249:617-636. Medline
39. Kleim JA, Barbay S, Nudo RJ (1998) Functional reorganization of the rat motor cortex following motor skill learning. J Neurophysiol 80:3321-3325. Medline
40. Kleim JA, Barbay S, Cooper NR, Hogg TM, Reidel CN, Remple MS, Nudo RJ (2002) Motor learning-dependent synaptogenesis is localized to functionally reorganized motor cortex. Neurobiol Learn Mem 77:63-77. CrossRef Medline
41. Kleim JA, Bruneau R, VandenBerg P, MacDonald E, Mulrooney R, Pocock D (2003) Motor cortex stimulation enhances motor recovery and reduces peri-infarct dysfunction following ischemic insult. Neurol Res 25:789-793. CrossRef Medline
42. Kleim JA, Hogg TM, VandenBerg PM, Cooper NR, Bruneau R, Remple M (2004) Cortical synaptogenesis and motor map reorganization occur during late, but not early, phase of motor skill learning. J Neurosci 24: 628-633. CrossRef Medline
43. Kruglikov I, Rudy B (2008) Perisomatic GABA release and thalamocortical integration onto neocortical excitatory cells are regulated by neuromodulators. Neuron 58:911-924. CrossRef Medline
44. Lambe EK, Goldman-Rakic PS, Aghajanian GK (2000) Serotonin induces EPSCs preferentially in layer V pyramidal neurons of the frontal cortex in rats. Cereb Cortex 10:974-980. CrossRef Medline
45. Lanfumey L, Haj-Dahmane S, Hamon M (1993) Further assessment of the antagonist properties of the novel and selective 5-HT1A receptor ligands (+)-WAY 100 135 and SDZ 216-525. Eur J Pharmacol 249:25-35. CrossRef Medline
46. Lee JK, Emch GS, Johnson CS, Wrathall JR (2005) Effect of spinal cord injury severity on alterations of the H-reflex. Exp Neurol 196:430-440. CrossRef Medline
47. Lladó-Pelfort L, Santana N, Ghisi V, Artigas F, Celada P (2012) 5-HT1A receptor agonists enhance pyramidal cell firing in prefrontal cortex through a preferential action on GABA interneurons. Cereb Cortex 22: 1487-1497. CrossRef Medline
48. Madriaga MA, McPhee LC, Chersa T, Christie KJ, Whelan PJ (2004) Modulation of locomotor activity by multiple 5-HT and dopaminergic receptor subtypes in the neonatal mouse spinal cord. J Neurophysiol 92:1566-1576. CrossRef Medline
49. Metz GA, Piecharka DM, Kleim JA, Whishaw IQ (2004) Preserved ipsilateral-to-lesion motor map organization in the unilateral 6-OHDAtreated rat model of Parkinson's disease. Brain Res 1026:126-135. CrossRef Medline
50. Monfils MH, VandenBerg PM, Kleim JA, Teskey GC (2004) Long-term potentiation induces expanded movement representations and dendritic hypertrophy in layer V of rat sensorimotor cortex. Cereb Cortex 14:586-593. CrossRef Medline
51. Moore RY, Halaris AE, Jones BE (1978) Serotonin neurons of the midbrain raphe: ascending projections. J Comp Neurol 180:417-438. CrossRef Medline
52. Nakai K, Fujii T, Fujimoto K, Suzuki T, Kawashima K (1998) Effect of WAY-100135 on the hippocampal acetylcholine release potentiated by 8-OH DPAT, a serotonin 1A receptor agonist, in normal and p-chlorophenylalanine-treated rats as measured by the in vivo microdialysis. Neurosci Res 31:23-29. CrossRef Medline
53. Nudo RJ, Jenkins WM, Merzenich MM (1990) Repetitive microstimulation alters the cortical representation of movements in adult rats. Somatosens Mot Res 7:463-483. CrossRef Medline
54. Parks CL, Robinson PS, Sibille E, Shenk T, Toth M (1998) Increased anxiety of mice lacking the serotonin1A receptor. Proc Natl Acad Sci U S A 95: 10734-10739. CrossRef Medline
55. Pflieger JF, Clarac F, Vinay L (2002) Postural modifications and neuronal excitability changes induced by a short-term serotonin depletion during neonatal development in the rat. J Neurosci 22:5108-5117. Medline
56. Povysheva NV, Gonzalez-Burgos G, Zaitsev AV, Kröner S, Barrionuevo G, Lewis DA, Krimer LS (2006) Properties of excitatory synaptic responses in fast-spiking interneurons and pyramidal cells from monkey and rat prefrontal cortex. Cereb Cortex 16:541-552. Medline
57. Puig MV, Artigas F, Celada P (2005) Modulation of the activity of pyramidal neurons in rat prefrontal cortex by raphe stimulation in vivo: involvement of serotonin and GABA. Cereb Cortex 15:1-14. Medline
58. Puig MV, Watakabe A, Ushimaru M, Yamamori T, Kawaguchi Y (2010) Serotonin modulates fast-spiking interneuron and synchronous activity in the rat prefrontal cortex through 5-HT1A and 5-HT2A receptors. J Neurosci 30:2211-2222. CrossRef Medline
59. Ramanathan D, Tuszynski MH, Conner JM (2009) The basal forebrain cholinergic system is required specifically for behaviorally mediated cortical map plasticity. J Neurosci 29:5992-6000. CrossRef Medline
60. Rathelot JA, Strick PL (2006) Muscle representation in the macaque motor cortex: an anatomical perspective. Proc Natl Acad Sci U S A 103:8257-8262. CrossRef Medline
61. Ruat M, Traiffort E, Leurs R, Tardivel-Lacombe J, Diaz J, Arrang JM, Schwartz JC (1993) Molecular cloning, characterization, and localization of a high-affinity serotonin receptor (5-HT7) activating cAMP formation. Proc Natl Acad Sci U S A 90:8547-8551. CrossRef Medline
62. Schmidt BJ, Jordan LM (2000) The role of serotonin in reflex modulation and locomotor rhythm production in the mammalian spinal cord. Brain Res Bull 53:689-710. CrossRef Medline
63. Smith VM, Sterniczuk R, Phillips CI, Antle MC (2008) Altered photic and nonphotic phase shifts in 5-HT(1A) receptor knockout mice. Neuroscience 157:513-523. CrossRef Medline
64. Strick PL (2002) Stimulating research on motor cortex. Nat Neurosci 5:714-715. CrossRef Medline
65. Tennant KA, Adkins DL, Donlan NA, Asay AL, Thomas N, Kleim JA, Jones TA (2011) The organization of the forelimb representation of the C57BL/6 mouse motor cortex as defined by intracortical microstimulation and cytoarchitecture. Cereb Cortex 21:865-876. CrossRef Medline
66. Teskey GC, Young NA, van Rooyen F, Larson SE, Flynn C, Monfils MH, Kleim JA, Henry LC, Goertzen CD (2007) Induction of neocortical long-term depression results in smaller movement representations, fewer excitatory perforated synapses and more inhibitory synapses. Cereb Cortex 17:434-442. Medline
67. Vanderwolf CH (1989) A general role for serotonin in the control of behavior: studies with intracerebral 5,7-dihydroxytryptamine. Brain Res 504: 192-198. CrossRef Medline
68. Whishaw IQ (2000) Loss of the innate cortical engram for action patterns used in skilled reaching and the development of behavioural compensation following motor cortex lesions in the rat. Neuropharmacology 39: 788-805. CrossRef Medline
69. Whishaw IQ, Pellis SM, Pellis VC (1992) A behavioural study of the contributions of cells and fibers of passage in the red nucleus of the rat to postural righting, skilled movements, and learning. Behav Brain Res 52: 29-44. CrossRef Medline
70. Whishaw IQ, Pellis SM, Gorny B, Kolb B, Tetzlaff W (1993) Proximal and distal impairments in rat forelimb use in reaching follow unilateral pyramidal tract lesions. Behav Brain Res 56:59-76. CrossRef Medline
71. Whishaw IQ, Gorny B, Foroud A, Kleim JA (2003) Long-Evans and Sprague-Dawley rats have similar skilled reaching success and limb representations in motor cortex but different movements: some cautionary insights into the selection of rat strains for neurobiological motor research. Behav Brain Res 145:221-232. CrossRef Medline
72. Whishaw IQ, Zeeb F, Erickson C, McDonald RJ (2007) Neurotoxic lesions of the caudate-putamen on a reaching for food task in the rat: acute sensorimotor neglect and chronic qualitative motor impairment follow lateral lesions and improved success follows lateral lesions and improved success follows medial lesions. Neuroscience 146:86-97. CrossRef Medline
73. White SR, Fung SJ, Jackson DA, Imel KM (1996) Serotonin, norepinephrine and associated neuropeptides: effects on somatic motor neuron excitability. Prog Brain Res 107:183-199. CrossRef Medline
74. Young NA, Vuong J, Flynn C, Teskey GC (2011) Optimal parameters for microstimulation derived forelimb movement thresholds and motor maps in rats and mice. J Neurosci Methods 196:60-69. CrossRef Medline