Synchronized firing of fast-spiking interneurons is critical to maintain balanced firing between direct and indirect pathway neurons of the striatum

Journal of Neurophysiology

Volumn 111, Issue 4, 2014, Pages 836-848

  Damodaran, Sriraman ^a   Evans, Rebekah C ^a   Blackwell, Kim T ^a  

^a GEORGE MASON UNIVERSITY   (United States)

Author keywords

Fast spiking interneuron; Gap junctions; Medium spiny neuron; Parkinson's disease; Striatum

Indexed keywords

FAST-SPIKING INTERNEURON; GAP JUNCTIONS; MEDIUM-SPINY NEURON; PARKINSON'S DISEASE; STRIATUM;

ACTION POTENTIALS; ANIMALS; CEREBRAL CORTEX; CORPUS STRIATUM; FEMALE; INTERNEURONS; MALE; MICE; MICE, INBRED C57BL; MODELS, NEUROLOGICAL; NEURAL INHIBITION; SYNAPTIC POTENTIALS; TIME FACTORS;

EID: 84894093609     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00382.2013     Document Type: Article

References (66)

1. Albin RL, Young AB, Penney JB. The functional anatomy of basal ganglia disorders. Trends Neurosci 12: 366-375, 1989.
2. Bennett BD, Bolam JP. Synaptic input and output of parvalbumin-immunoreactive neurons in the neostriatum of the rat. Neuroscience 62: 707-719, 1994.
3. Berke JD, Okatan M, Skurski J, Eichenbaum HB. Oscillatory entrainment of striatal neurons in freely moving rats. Neuron 43: 883-896, 2004.
4. Berke JD. Fast oscillations in cortical-striatal networks switch frequency following rewarding events and stimulant drugs. Eur J Neurosci 30: 848-859, 2009.
5. Blackwell KT, Czubayko U, Plenz D. Quantitative estimate of synaptic inputs to striatal neurons during up and down states in vitro. J Neurosci 23: 9123-9132, 2003.
6. Bower JM, Beeman D. Constructing realistic neural simulations with GENESIS. Methods Mol Biol 401: 103-125, 2007.
7. Bracci E, Centonze D, Bernardi G, Calabresi P. Dopamine excites fastspiking interneurons in the striatum. J Neurophysiol 87: 2190-2194, 2002.
8. Burkhardt JM, Constantinidis C, Anstrom KK, Roberts DCS, Woodward DJ. Synchronous oscillations and phase reorganization in the basal ganglia during akinesia induced by high-dose haloperidol. Eur J Neurosci 26: 1912-1924, 2007.
9. Carrillo-Reid L, Tecuapetla F, Tapia D, Hernández-Cruz A, Galarraga E, Drucker-Colin R, Bargas J. Encoding network states by striatal cell assemblies. J Neurophysiol 99: 1435-1450, 2008.
10. Centonze D, Grande C, Usiello A, Gubellini P, Erbs E, Martin AB, Pisani A, Tognazzi N, Bernardi G, Moratalla R, Borrelli E, Calabresi P. Receptor subtypes involved in the presynaptic and postsynaptic actions of dopamine on striatal interneurons. J Neurosci 23: 6245-6254, 2003.
11. Chan CS, Peterson JD, Gertler TS, Glajch KE, Quintana RE, Cui Q, Sebel LE, Plotkin JL, Shen W, Heiman M, Heintz N, Greengard P, Surmeier DJ. Strain-specific regulation of striatal phenotype in Drd2-eGFP BAC transgenic mice. J Neurosci 32: 9124-9132, 2012.
12. Costa RM, Lin SC, Sotnikova TD, Cyr M, Gainetdinov RR, Caron MG, Nicolelis MAL. Rapid alterations in corticostriatal ensemble coordination during acute dopamine-dependent motor dysfunction. Neuron 52: 359-369, 2006.
13. Cui G, Jun SB, Jin X, Pham MD, Vogel SS, Lovinger DM, Costa RM. Concurrent activation of striatal direct and indirect pathways during action initiation. Nature 494: 238-242, 2013.
14. Day M, Wang Z, Ding J, An X, Ingham CA, Shering AF, Wokosin D, Ilijic E, Sun Z, Sampson AR, Mugnaini E, Deutch AY, Sesack SR, Arbuthnott GW, Surmeier DJ. Selective elimination of glutamatergic synapses on striatopallidal neurons in Parkinson disease models. Nat Neurosci 9: 251-259, 2006.
15. DeLong MR. Primate models of movement disorders of basal ganglia origin. Trends Neurosci 13: 281-285, 1990.
16. Ding J, Peterson JD, Surmeier DJ. Corticostriatal and thalamostriatal synapses have distinctive properties. J Neurosci 28: 6483-6492, 2008.
17. Edgerton JR, Hanson JE, Günay C, Jaeger D. Dendritic sodium channels regulate network integration in globus pallidus neurons: a modeling study. J Neurosci 30: 15146-15159, 2010.
18. Erisir A, Lau D, Rudy B, Leonard CS. Function of specific K(+) channels in sustained high-frequency firing of fast-spiking neocortical interneurons. J Neurophysiol 82: 2476-2489, 1999.
19. Evans RC, Morera-Herreras T, Cui Y, Du K, Sheehan T, Kotaleski JH, Venance L, Blackwell KT. The effects of NMDA subunit composition on calcium influx and spike timing-dependent plasticity in striatal medium spiny neurons. PLoS Comput Biol 8: e1002493, 2012.
20. Flores-Barrera E, Vizcarra-Chacón BJ, Bargas J, Tapia D, Galarraga E. Dopaminergic modulation of corticostriatal responses in medium spiny projection neurons from direct and indirect pathways. Front Syst Neurosci 5: 15, 2011.
21. Freund TF, Powell JF, Smith AD. Tyrosine hydroxylase-immunoreactive boutons in synaptic contact with identified striatonigral neurons, with particular reference to dendritic spines. Neuroscience 13: 1189-1215, 1984.
22. Galarreta M, Hestrin S. Electrical and chemical synapses among parvalbumin fast-spiking GABAergic interneurons in adult mouse neocortex. Proc Natl Acad Sci U S A 99: 12438-12443, 2002.
23. Gertler TS, Chan CS, Surmeier DJ. Dichotomous anatomical properties of adult striatal medium spiny neurons. J Neurosci 28: 10814-10824, 2008.
24. Gittis AH, Hang GB, LaDow ES, Shoenfeld LR, Atallah BV, Finkbeiner S, Kreitzer AC. Rapid target-specific remodeling of fast-spiking inhibitory circuits after loss of dopamine. Neuron 71: 858-868, 2011a.
25. Gittis AH, Leventhal DK, Fensterheim BA, Pettibone JR, Berke JD, Kreitzer AC. Selective inhibition of striatal fast-spiking interneurons causes dyskinesias. J Neurosci 31: 15727-15731, 2011b.
26. Gittis AH, Nelson AB, Thwin MT, Palop JJ, Kreitzer AC. Distinct roles of GABAergic interneurons in the regulation of striatal output pathways. J Neurosci 30: 2223-2234, 2010.
27. 2+ influx by D2 dopamine and A2A adenosine receptors. Nat Neurosci 13: 958-966, 2010.
28. Hikosaka O, Takikawa Y, Kawagoe R. Role of the basal ganglia in the control of purposive saccadic eye movements. Physiol Rev 80: 953-978, 2000.
29. Hjorth J, Blackwell KT, Kotaleski JH. Gap junctions between striatal fast-spiking interneurons regulate spiking activity and synchronization as a function of cortical activity. J Neurosci 29: 5276-5286, 2009.
30. Humphries MD, Wood R, Gurney K. Dopamine-modulated dynamic cell assemblies generated by the GABAergic striatal microcircuit. Neural Netw 22: 1174-1188, 2009.
31. Kita H, Kosaka T, Heizmann CW. Parvalbumin-immunoreactive neurons in the rat neostriatum: a light and electron microscopic study. Brain Res 536: 1-15, 1990.
32. Kita H. Glutamatergic and GABAergic postsynaptic responses of striatal spiny neurons to intrastriatal and cortical stimulation recorded in slice preparations. Neuroscience 70: 925-940, 1996.
33. Koos T, Tepper JM, Wilson CJ. Comparison of IPSCs evoked by spiny and fast-spiking neurons in the neostriatum. J Neurosci 24: 7916-7922, 2004.
34. Koós T, Tepper JM. Inhibitory control of neostriatal projection neurons by GABAergic interneurons. Nat Neurosci 2: 467-472, 1999.
35. Kotaleski JH, Plenz D, Blackwell KT. Using potassium currents to solve signal-to-noise problems in inhibitory feedforward networks of the striatum. J Neurophysiol 95: 331-341, 2006.
36. Kravitz AV, Freeze BS, Parker PRL, Kay K, Thwin MT, Deisseroth K, Kreitzer AC. Regulation of Parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 466: 622-626, 2010.
37. Kreitzer AC, Malenka RC. Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson's disease models. Nature 445: 643-647, 2007.
38. Krüger J, Aiple F. Multimicroelectrode investigation of monkey striate cortex: spike train correlations in the infragranular layers. J Neurophysiol 60: 798-828, 1988.
39. Lau T, Gage GJ, Berke JD, Zochowski M. Local dynamics of gap-junctioncoupled interneuron networks. Phys Biol 7: 16015, 2010.
40. Logan SM, Partridge JG, Matta JA, Buonanno A, Vicini S. Long-lasting NMDA receptor-mediated EPSCs in mouse striatal medium spiny neurons. J Neurophysiol 98: 2693-2704, 2007.
41. Mallet N, Ballion B, Le Moine C, Gonon F. Cortical inputs and GABA interneurons imbalance projection neurons in the striatum of parkinsonian rats. J Neurosci 26: 3875-3884, 2006.
42. Mallet N, Micklem BR, Henny P, Brown MT, Williams C, Bolam JP, Nakamura KC, Magill PJ. Dichotomous organization of the external globus pallidus. Neuron 74: 1075-1086, 2012.
43. Mallet N, Pogosyan A, Márton LF, Bolam JP, Brown P, Magill PJ. Parkinsonian beta oscillations in the external globus pallidus and their relationship with subthalamic nucleus activity. J Neurosci 28: 14245-14258, 2008.
44. Mercuri NB, Calabresi P, Stefani A, Stratta F, Bernardi G. GABA depolarizes neurons in the rat striatum: an in vivo study. Synapse 8: 38-40, 1991.
45. Moyer JT, Wolf JA, Finkel LH. Effects of dopaminergic modulation on the integrative properties of the ventral striatal medium spiny neuron. J Neurophysiol 98: 3731-3748, 2007.
46. Nicola SM, Surmeier J, Malenka RC. Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. Annu Rev Neurosci 23: 185-215, 2000.
47. Obeso JA, Rodriguez-Oroz M, Marin C, Alonso F, Zamarbide I, Lanciego JL, Rodriguez-Diaz M. The origin of motor fluctuations in Parkinson's disease: importance of dopaminergic innervation and basal ganglia circuits. Neurology 62: S17-S30, 2004.
48. Oorschot DE, Lin N, Cooper BH, Reynolds JNJ, Sun H, Wickens JR. Local connectivity between rat striatal spiny projection neurons: a threedimensional ultrastructural study of somal innervation. IBAGS X. New Jersey: 2010, p. 114.
49. Planert H, Szydlowski SN, Hjorth JJJ, Grillner S, Silberberg G. Dynamics of synaptic transmission between fast-spiking interneurons and striatal projection neurons of the direct and indirect pathways. J Neurosci 30: 3499-3507, 2010.
50. Plenz D. When inhibition goes incognito: feedback interaction between spiny projection neurons in striatal function. Trends Neurosci 26: 436-443, 2003.
51. Ponzi A, Wickens J. Sequentially switching cell assemblies in random inhibitory networks of spiking neurons in the striatum. J Neurosci 30: 5894-5911, 2010.
52. Popescu AT, Saghyan AA, Paré D. NMDA-dependent facilitation of corticostriatal plasticity by the amygdala. Proc Natl Acad Sci U S A 104: 341-346, 2007.
53. Ramanathan S, Hanley JJ, Deniau JM, Bolam JP. Synaptic convergence of motor and somatosensory cortical afferents onto GABAergic interneurons in the rat striatum. J Neurosci 22: 8158-8169, 2002.
54. Stern EA, Jaeger D, Wilson CJ. Membrane potential synchrony of simultaneously recorded striatal spiny neurons in vivo. Nature 394: 475-478, 1998.
55. Surmeier DJ, Ding J, Day M, Wang Z, Shen W. D1 and D2 dopaminereceptor modulation of striatal glutamatergic signaling in striatal medium spiny neurons. Trends Neurosci 30: 228-235, 2007.
56. Taverna S, Ilijic E, Surmeier DJ. Recurrent collateral connections of striatal medium spiny neurons are disrupted in models of Parkinson's disease. J Neurosci 28: 5504-5512, 2008.
57. Tecuapetla F, Carrillo-Reid L, Bargas J, Galarraga E. Dopaminergic modulation of short-term synaptic plasticity at striatal inhibitory synapses. Proc Natl Acad Sci U S A 104: 10258-10263, 2007.
58. Tepper JM, Lee CR. GABAergic control of substantia nigra dopaminergic neurons. Prog Brain Res 160: 189-208, 2007.
59. Traub RD, Kopell N, Bibbig A, Buhl EH, LeBeau FE, Whittington MA. Gap junctions between interneuron dendrites can enhance synchrony of gamma oscillations in distributed networks. J Neurosci 21: 9478-9486, 2001.
60. Trevitt JT, Morrow J, Marshall JF. Dopamine manipulation alters immediate-early gene response of striatal parvalbumin interneurons to cortical stimulation. Brain Res 1035: 41-50, 2005.
61. Ts'o DY, Gilbert CD. The organization of chromatic and spatial interactions in the primate striate cortex. J Neurosci 8: 1712-1727, 1988.
62. Tunstall MJ, Oorschot DE, Kean A, Wickens JR. Inhibitory interactions between spiny projection neurons in the rat striatum. J Neurophysiol 88: 1263-1269, 2002.
63. Wilson CJ. Postsynaptic potentials evoked in spiny neostriatal projection neurons by stimulation of ipsilateral and contralateral neocortex. Brain Res 367: 201-213, 1986.
64. Wilson CJ, Chang HT, Kitai ST. Firing patterns and synaptic potentials of identified giant aspiny interneurons in the rat neostriatum. J Neurosci 10: 508-519, 1990.
65. Wilson CJ, Kawaguchi Y. The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons. J Neurosci 16: 2397-2410, 1996.
66. Yim MY, Aertsen A, Kumar A. Significance of input correlations in striatal function. PLoS Comput Biol 7: e1002254, 2011.