Relationships between the firing of identified striatal interneurons and spontaneous and driven cortical activities in vivo

Journal of Neuroscience

Volumn 32, Issue 38, 2012, Pages 13221-13236

  Sharott, Andrew ^a   Doig, Natalie M ^a   Mallet, Nicolas ^a   Magill, Peter J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CHOLINE ACETYLTRANSFERASE; NEUROBIOTIN; NEURONAL TRACT TRACER; NITRIC OXIDE SYNTHASE; PARVALBUMIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CALCIUM CURRENT; CHOLINERGIC NERVE CELL; ELECTROCORTICOGRAPHY; ELECTROENCEPHALOGRAM; ELECTROPHYSIOLOGY; ELECTROSTIMULATION; GABAERGIC SYSTEM; GAMMA RHYTHM; IMMUNOFLUORESCENCE TEST; INTERNEURON; MALE; MOTOR CORTEX; NERVE CELL NETWORK; NERVE PROJECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SOMATOSENSORY STIMULATION; STRIATE CORTEX;

ACTION POTENTIALS; ANIMALS; BIOTIN; BRAIN WAVES; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CEREBRAL CORTEX; CHOLINE O-ACETYLTRANSFERASE; CORPUS STRIATUM; ELECTRIC STIMULATION; ELECTROCARDIOGRAPHY; FUNCTIONAL LATERALITY; HINDLIMB; INTERNEURONS; MALE; NEURAL PATHWAYS; NEUROPEPTIDE Y; NITRIC OXIDE SYNTHASE; PARVALBUMINS; PHYSICAL STIMULATION; RATS; RATS, SPRAGUE-DAWLEY; STATISTICS, NONPARAMETRIC;

EID: 84866402339     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2440-12.2012     Document Type: Article

References (68)

1. Beatty JA, Sullivan MA, Morikawa H, Wilson CJ (2012) Complex autonomous firing patterns of striatal low-threshold spike interneurons. J Neu-rophysiol 108:771-781.
2. Bennett BD, Wilson CJ (1999) Spontaneous activity of neostriatal cholinergic interneurons in vitro. J Neurosci 19:5586-5596.
3. Berens P (2009) CircStat: A MATLAB Toolbox for Circular Statistics. J Statistical Software 31:1-21.
4. Berke JD (2011) Functional properties of striatal fast-spiking interneurons. Front Syst Neurosci 5:45.
5. Berke JD (2009) Fast oscillations in cortical-striatal networks switch frequency following rewarding events and stimulant drugs. Eur J Neurosci 30:848-859.
6. Berke JD, Okatan M, Skurski J, Eichenbaum HB (2004) Oscillatory entrainment of striatal neurons in freely moving rats. Neuron 43:883-896.
7. Centonze D, Bracci E, Pisani A, Gubellini P, Bernardi G, Calabresi P (2002) Activation of dopamine D1-like receptors excites LTS interneurons of the striatum. Eur J Neurosci 15:2049-2052.
8. Costa RM, Lin SC, Sotnikova TD, Cyr M, Gainetdinov RR, Caron MG, Nicolelis MA (2006) Rapid alterations in corticostriatal ensemble coordination during acute dopamine-dependent motor dysfunction. Neuron 52:359-369.
9. DeCoteau WE, Thorn C, Gibson DJ, Courtemanche R, Mitra P, Kubota Y, Graybiel AM (2007) Learning-related coordination of striatal and hippocampal theta rhythms during acquisition of a procedural maze task. Proc Natl Acad Sci U S A 104:5644-5649.
10. Deffains M, Legallet E, Apicella P (2010) Modulation of neuronal activity in the monkey putamen associated with changes in the habitual order of sequential movements. J Neurophysiol 104:1355-1369.
11. Ding JB, Guzman JN, Peterson JD, Goldberg JA, Surmeier DJ (2010) Thalamic gating of corticostriatal signaling by cholinergic interneurons. Neuron 67:294-307.
12. Domich L, Oakson G, Steriade M (1986) Thalamic burst patterns in the naturally sleeping cat: a comparison between cortically projecting and reticularis neurones. J Physiol 379:429-449.
13. Eusebio A, Pogosyan A, Wang S, Averbeck B, Gaynor LD, Cantiniaux S, Witjas T, Limousin P, Azulay JP, Brown P (2009) Resonance in subthalamo-cortical circuits in Parkinson's disease. Brain 132:2139-2150.
14. Fanselow EE, Sameshima K, Baccala LA, Nicolelis MA (2001) Thalamic bursting in rats during different awake behavioral states. Proc Natl Acad Sci U S A 98:15330-15335.
15. Figueredo-Cardenas G, Morello M, Sancesario G, Bernardi G, Reiner A (1996) Colocalization of somatostatin, neuropeptide Y, neuronal nitric oxide synthase and NADPH-diaphorase in striatal interneurons in rats. Brain Res 735:317-324.
16. Gittis AH, Nelson AB, Thwin MT, Palop JJ, Kreitzer AC (2010) Distinct roles of GABAergic interneurons in the regulation of striatal output path-ways. J Neurosci 30:2223-2234.
17. Goldberg JA, Reynolds JN (2011) Spontaneous firing and evoked pauses in the tonically active cholinergic interneurons of the striatum. Neurosci-ence 198:27-43.
18. Hasenstaub A, Shu Y, Haider B, Kraushaar U, Duque A, McCormick DA (2005) Inhibitory postsynaptic potentials carry synchronized frequency information in active cortical networks. Neuron 47:423-435.
19. Holt GR, Softky WR, Koch C, Douglas RJ (1996) Comparison of discharge variability in vitro and in vivo in cat visual cortex neurons. J Neurophysiol 75:1806-1814.
20. Ibáñez-Sandoval O, Tecuapetla F, Unal B, Shah F, Koós T, Tepper JM (2010) Electrophysiological and morphological characteristics and synaptic connectivity of tyrosine hydroxylase-expressing neurons in adult mouse striatum. J Neurosci 30:6999-7016.
21. Ibáñez-Sandoval O, Tecuapetla F, Unal B, Shah F, Koós T, Tepper JM (2011) A novel functionally distinct subtype of striatal neuropeptide Y interneuron. J Neurosci 31:16757-16769.
22. Inokawa H, Yamada H, Matsumoto N, Muranishi M, Kimura M (2010) Juxtacellular labeling of tonically active neurons and phasically active neurons in the rat striatum. Neuroscience 168:395-404.
23. Isomura Y, Harukuni R, Takekawa T, Aizawa H, Fukai T (2009) Microcircuitry coordination of cortical motor information in self-initiation of voluntary movements. Nat Neurosci 12:1586-1593.
24. Jeanmonod D, Magnin M, Morel A (1996) Low-threshold calcium spike bursts in the human thalamus. Common physiopathology for sensory, motor and limbic positive symptoms. Brain 119:363-375.
25. Joshua M, Adler A, Mitelman R, Vaadia E, Bergman H (2008) Midbrain dopaminergic neurons and striatal cholinergic interneurons encode the difference between reward and aversive events at different epochs of probabilistic classical conditioning trials. J Neurosci 28:11673-11684.
26. Kawaguchi Y (1993) Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum. J Neurosci 13:4908-4923.
27. Kimura M, Rajkowski J, Evarts E (1984) Tonically discharging putamen neurons exhibit set-dependent responses. Proc Natl Acad Sci U S A 81:4998-5001.
28. Kimura M, Kato M, Shimazaki H, Watanabe K, Matsumoto N (1996) Neural information transferred from the putamen to the globus pallidus during learned movement in the monkey. J Neurophysiol 76:3771-3786.
29. Kita H, Kosaka T, Heizmann CW (1990) Parvalbumin-immunoreactive neurons in the rat neostriatum: a light and electron microscopic study. Brain Res 536:1-15.
30. Kolomiets BP, Deniau JM, Glowinski J, Thierry AM (2003) Basal ganglia and processing of cortical information: functional interactions between trans-striatal and trans-subthalamic circuits in the substantia nigra pars reticulata. Neuroscience 117:931-938.
31. Koós T, Tepper JM (1999) Inhibitory control of neostriatal projection neurons by GABAergic interneurons. Nat Neurosci 2:467-472.
32. Kubota Y, Mikawa S, Kawaguchi Y (1993) Neostriatal GABAergic interneurones contain NOS, calretinin or parvalbumin. Neuroreport 5:205-208.
33. Lacey CJ, Bolam JP, Magill PJ (2007) Novel and distinct operational principles of intralaminar thalamic neurons and their striatal projections. J Neurosci 27:4374-4384.
34. Lachaux JP, Rodriguez E, Martinerie J, Varela FJ (1999) Measuring phase synchrony in brain signals. Hum Brain Mapp 8:194-208.
35. Lapper SR, Bolam JP (1992) Input from the frontal cortex and the parafascicular nucleus to cholinergic interneurons in the dorsal striatum of the rat. Neuroscience 51:533-545.
36. Leventhal DK, Gage GJ, Schmidt R, Pettibone JR, Case AC, Berke JD (2012) Basal ganglia beta oscillations accompany cue utilization. Neuron 73:523-536.
37. Lu SM, Guido W, Sherman SM (1992) Effects of membrane voltage on receptive field properties of lateral geniculate neurons in the cat: contributions of the low-threshold Ca2 conductance. J Neurophysiol 68:2185-2198.
38. Magill PJ, Bolam JP, Bevan MD (2000) Relationship of activity in the subthalamic nucleus-globus pallidus network to cortical electroencephalogram. J Neurosci 20:820-833.
39. Magill PJ, Sharott A, Bolam JP, Brown P (2004a) Brain state-dependency of coherent oscillatory activity in the cerebral cortex and basal ganglia of the rat. J Neurophysiol 92:2122-2136.
40. Magill PJ, Sharott A, Bevan MD, Brown P, Bolam JP (2004b) Synchronous unit activity and local field potentials evoked in the subthalamic nucleus by cortical stimulation. J Neurophysiol 92:700-714.
41. Magill PJ, Pogosyan A, Sharott A, Csicsvari J, Bolam JP, Brown P (2006) Changes in functional connectivity within the rat striatopallidal axis during global brain activation in vivo. J Neurosci 26:6318-6329.
42. Mallet N, Le Moine C, Charpier S, Gonon F (2005) Feedforward inhibition of projection neurons by fast-spiking GABA interneurons in the rat striatum in vivo. J Neurosci 25:3857-3869.
43. Mallet N, Pogosyan A, Márton LF, Bolam JP, Brown P, Magill PJ (2008) Parkinsonian beta oscillations in the external globus pallidus and their relationship with subthalamic nucleus activity. J Neurosci 28:14245-14258.
44. Mallet N, Micklem BR, Henny P, Brown MT, Williams C, Bolam JP, Nakamura KC, Magill PJ (2012) Dichotomous organization of the external globus pallidus. Neuron 74:1075-1086.
45. Morello M, Reiner A, Sancesario G, Karle EJ, Bernardi G (1997) Ultrastructural study of nitric oxide synthase-containing striatal neurons and their relationship with parvalbumin-containing neurons in rats. Brain Res 776:30-39.
46. Morris G, Arkadir D, Nevet A, Vaadia E, Bergman H (2004) Coincident but distinct messages of midbrain dopamine and striatal tonically active neurons. Neuron 43:133-143.
47. Nambu A (2008) Seven problems on the basal ganglia. Curr Opin Neurobiol 18:595-604.
48. Ondracek JM, Dec A, Hoque KE, Lim SA, Rasouli G, Indorkar RP, Linardakis J, Klika B, Mukherji SJ, Burnazi M, Threlfell S, Sammut S, West AR (2008) Feed-forward excitation of striatal neuron activity by frontal cortical activation of nitric oxide signaling in vivo. Eur J Neurosci 27:1739-1754.
49. Paladini CA, Tepper JM (1999) GABA(A) and GABA(B) antagonists differentially affect the firing pattern of substantia nigra dopaminergic neurons in vivo. Synapse 32:165-176.
50. Partridge JG, Janssen MJ, Chou DY, Abe K, Zukowska Z, Vicini S (2009) Excitatory and inhibitory synapses in neuropeptide Y-expressing striatal interneurons. J Neurophysiol 102:3038-3045.
51. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates, Ed 2. Sydney: Academic Press.
52. Ramanathan S, Hanley JJ, Deniau JM, Bolam JP (2002) Synaptic convergence of motor and somatosensory cortical afferents onto GABAergic Interneurons in the rat striatum. J Neurosci 22:8158-8169.
53. Reynolds JN, Wickens JR (2004) The corticostriatal input to giant aspiny interneurons in the rat: a candidate pathway for synchronising the response to reward-related cues. Brain Res 1011:115-128.
54. Saleem AB, Chadderton P, Apergis-Schoute J, Harris KD, Schultz SR (2010) Methods for predicting cortical UP and DOWN states from the phase of deep layer local field potentials. J Comput Neurosci 29:49-62.
55. Sammut S, Park DJ, West AR (2007) Frontal cortical afferents facilitate striatal nitric oxide transmission in vivo via a NMDA receptor and neuronal NOS-dependent mechanism. J Neurochem 103:1145-1156.
56. Sammut S, Threlfell S, West AR (2010) Nitric oxide-soluble guanylyl cyclase signaling regulates corticostriatal transmission and short-term synaptic plasticity of striatal projection neurons recorded in vivo. Neuropharmacology 58:624-631.
57. Schulz JM, Oswald MJ, Reynolds JN (2011a) Visual-induced excitation leads to firing pauses in striatal cholinergic interneurons. J Neurosci 31:11133-11143.
58. Schulz JM, Pitcher TL, Savanthrapadian S, Wickens JR, Oswald MJ, Reynolds JN (2011b) Enhanced high-frequency membrane potential fluctuations control spike output in striatal fast-spiking interneurones in vivo. J Physiol 589:4365-4381.
59. Sciamanna G, Tassone A, Martella G, Mandolesi G, Puglisi F, Cuomo D, Madeo G, Ponterio G, Standaert DG, Bonsi P, Pisani A (2011) Developmental profile of the aberrant dopamine D2 receptor response in striatal cholinergic interneurons in DYT1 dystonia. PLoS One 6:e24261.
60. Sharott A, Magill PJ, Bolam JP, Brown P (2005) Directional analysis of coherent oscillatory field potentials in the cerebral cortex and basal ganglia of the rat. J Physiol 562:951-963.
61. Sharott A, Moll CK, Engler G, Denker M, Grun S, Engel AK (2009) Different subtypes of striatal neurons are selectively modulated by cortical oscillations. J Neurosci 29:4571-4585.
62. Steriade M (2000) Corticothalamic resonance, states of vigilance and mentation. Neuroscience 101:243-276.
63. Stern EA, Kincaid AE, Wilson CJ (1997) Spontaneous subthreshold membrane potential fluctuations and action potential variability of rat corticostriatal and striatal neurons in vivo. J Neurophysiol 77:1697-1715.
64. Tepper JM, Bolam JP (2004) Functional diversity and specificity of neostriatal interneurons. Curr Opin Neurobiol 14:685-692.
65. Tepper JM, Tecuapetla F, Koós T, Ibáñez-Sandoval O (2010) Heterogeneity and diversity of striatal GABAergic interneurons. Front Neuroanat 4:150.
66. van der Meer MA, Redish AD (2009) Low and high gamma oscillations in rat ventral striatum have distinct relationships to behavior, reward, and spiking activity on a learned spatial decision task. Front Integr Neurosci 3:9.
67. Vuillet J, Kerkerian L, Salin P, Nieoullon A (1989) Ultrastructural features of NPY-containing neurons in the rat striatum. 477:241-251.
68. Wilson CJ, Chang HT, Kitai ST (1990) Firing patterns and synaptic potentials of identified giant aspiny interneurons in the rat neostriatum. J Neurosci 10:508-519.