 |
||||
|
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
The Journal of Neuroscience, January 1, 1998, 18(1):266-283
Up and Down States in Striatal Medium Spiny Neurons Simultaneously Recorded with Spontaneous Activity in Fast-Spiking Interneurons Studied in Cortex-Striatum-Substantia Nigra Organotypic Cultures
Dietmar Plenz and Stephen T. Kitai University of Tennessee, College of Medicine, Department of Anatomy and Neurobiology, Memphis, Tennessee 38163
In vivo intracellular spontaneous activity in striatal medium spiny (MS) projection neurons is characterized by "up" and "down" states. How this type of activity relates to the neuronal activity of striatal fast-spiking (FS) interneurons was examined in the presence of nigral and cortical inputs using cortex-striatum-substantia nigra organotypic cultures grown for 45 ± 4 d. The nigrostriatal projection was confirmed by tyrosine hydroxylase immunoreactivity. Corticostriatal (CS) projection neurons, striatal MS neurons, and FS neurons were intracellularly recorded and morphologically and electrophysiologically characterized. Intracellular spontaneous activity in the cultures consisted of intermittent depolarized periods of 0.5-1 sec duration. Spontaneous depolarizations in MS neurons were restricted to a narrow membrane potential range (up state) during which they occasionally fired single spikes. These up states were completely blocked by the glutamate antagonist CNQX. In FS interneurons, depolarized periods were characterized by large membrane potential fluctuations that occupied a wide range between rest and spike threshold. Also, FS interneurons spontaneously fired at much higher rates than did MS neurons. Simultaneous intracellular recordings established that during spontaneous depolarizations MS neurons and FS interneurons displayed correlated subthreshold neuronal activity in the low frequency range. These results indicate that (1) the CS projection neurons, striatal MS neurons, and FS interneurons grown in cortex-striatum-substantia nigra organotypic cultures show morphological and electrophysiological characteristics similar to those seen in vivo; (2) striatal MS neurons but not FS interneurons show an up state; (3) striatal MS neurons and FS interneurons receive common, presumably cortical inputs in the low frequency range. Our results support the view that the cortex provides a feedforward inhibition of MS neuron activity during the up state via FS interneurons.
Key words: cortex; striatum; substantia nigra; organotypic culture; corticostriatal projection; nigrostriatal projection; medium spiny projection neuron; fast-spiking interneuron; intracellular recording; cross-correlation
Copyright © 1998 Society for Neuroscience 0270-6474/98/181266-18$05.00/0
This article has been cited by other articles:
M. D\#8217;Ascenzo, M. V. Podda, T. Fellin, G. B. Azzena, P. Haydon, and C. Grassi
Activation of mGluR5 induces spike afterdepolarization and enhanced excitability in medium spiny neurons of the nucleus accumbens by modulating persistent Na+ currents
J. Physiol., July 1, 2009; 587(13): 3233 - 3250.
[Abstract] [Full Text] [PDF]
N. Dehorter, C. Guigoni, C. Lopez, J. Hirsch, A. Eusebio, Y. Ben-Ari, and C. Hammond
Dopamine-Deprived Striatal GABAergic Interneurons Burst and Generate Repetitive Gigantic IPSCs in Medium Spiny Neurons
J. Neurosci., June 17, 2009; 29(24): 7776 - 7787.
[Abstract] [Full Text] [PDF]
M. X Cohen, N. Axmacher, D. Lenartz, C. E. Elger, V. Sturm, and T. E. Schlaepfer
Nuclei Accumbens Phase Synchrony Predicts Decision-Making Reversals Following Negative Feedback
J. Neurosci., June 10, 2009; 29(23): 7591 - 7598.
[Abstract] [Full Text] [PDF]
M. Ishikawa, P. Mu, J. T. Moyer, J. A. Wolf, R. M. Quock, N. M. Davies, X.-t. Hu, O. M. Schluter, and Y. Dong
Homeostatic Synapse-Driven Membrane Plasticity in Nucleus Accumbens Neurons
J. Neurosci., May 6, 2009; 29(18): 5820 - 5831.
[Abstract] [Full Text] [PDF]
J. Hjorth, K. T. Blackwell, and J. Hellgren Kotaleski
Gap Junctions between Striatal Fast-Spiking Interneurons Regulate Spiking Activity and Synchronization as a Function of Cortical Activity
J. Neurosci., April 22, 2009; 29(16): 5276 - 5286.
[Abstract] [Full Text] [PDF]
B. R. Miller, A. G. Walker, A. S. Shah, S. J. Barton, and G. V. Rebec
Dysregulated Information Processing by Medium Spiny Neurons in Striatum of Freely Behaving Mouse Models of Huntington's Disease
J Neurophysiol, October 1, 2008; 100(4): 2205 - 2216.
[Abstract] [Full Text] [PDF]
J. D. Berke
Uncoordinated Firing Rate Changes of Striatal Fast-Spiking Interneurons during Behavioral Task Performance
J. Neurosci., October 1, 2008; 28(40): 10075 - 10080.
[Abstract] [Full Text] [PDF]
L. Liang, M. R. DeLong, and S. M. Papa
Inversion of Dopamine Responses in Striatal Medium Spiny Neurons and Involuntary Movements
J. Neurosci., July 23, 2008; 28(30): 7537 - 7547.
[Abstract] [Full Text] [PDF]
V. Pawlak and J. N. D. Kerr
Dopamine Receptor Activation Is Required for Corticostriatal Spike-Timing-Dependent Plasticity
J. Neurosci., March 5, 2008; 28(10): 2435 - 2446.
[Abstract] [Full Text] [PDF]
O. Darbin and T. Wichmann
Effects of Striatal GABAA-Receptor Blockade on Striatal and Cortical Activity in Monkeys
J Neurophysiol, March 1, 2008; 99(3): 1294 - 1305.
[Abstract] [Full Text] [PDF]
Y. H. Huang, Y. Lin, T. E. Brown, M.-H. Han, D. B. Saal, R. L. Neve, R. S. Zukin, B. A. Sorg, E. J. Nestler, R. C. Malenka, et al.
CREB Modulates the Functional Output of Nucleus Accumbens Neurons: A CRITICAL ROLE OF N-METHYL-D-ASPARTATE GLUTAMATE RECEPTOR (NMDAR) RECEPTORS
J. Biol. Chem., February 1, 2008; 283(5): 2751 - 2760.
[Abstract] [Full Text] [PDF]
E. Fino, J.-M. Deniau, and L. Venance
Cell-specific spike-timing-dependent plasticity in GABAergic and cholinergic interneurons in corticostriatal rat brain slices
J. Physiol., January 1, 2008; 586(1): 265 - 282.
[Abstract] [Full Text] [PDF]
J. K. H. Tang, E. Moro, N. Mahant, W. D. Hutchison, A. E. Lang, A. M. Lozano, and J. O. Dostrovsky
Neuronal Firing Rates and Patterns in the Globus Pallidus Internus of Patients With Cervical Dystonia Differ From Those With Parkinson's Disease
J Neurophysiol, August 1, 2007; 98(2): 720 - 729.
[Abstract] [Full Text] [PDF]
H. A. Johnson and D. V. Buonomano
Development and Plasticity of Spontaneous Activity and Up States in Cortical Organotypic Slices
J. Neurosci., May 30, 2007; 27(22): 5915 - 5925.
[Abstract] [Full Text] [PDF]
F. Kasanetz, L. A. Riquelme, P. O'Donnell, and M. G. Murer
Turning off cortical ensembles stops striatal Up states and elicits phase perturbations in cortical and striatal slow oscillations in rat in vivo
J. Physiol., November 15, 2006; 577(1): 97 - 113.
[Abstract] [Full Text] [PDF]
N. Petridou, D. Plenz, A. C. Silva, M. Loew, J. Bodurka, and P. A. Bandettini
Direct magnetic resonance detection of neuronal electrical activity
PNAS, October 24, 2006; 103(43): 16015 - 16020.
[Abstract] [Full Text] [PDF]
I. Freiman, A. Anton, H. Monyer, M. J. Urbanski, and B. Szabo
Analysis of the effects of cannabinoids on identified synaptic connections in the caudate-putamen by paired recordings in transgenic mice
J. Physiol., September 15, 2006; 575(3): 789 - 806.
[Abstract] [Full Text] [PDF]
N. Mallet, B. Ballion, C. Le Moine, and F. Gonon
Cortical inputs and GABA interneurons imbalance projection neurons in the striatum of parkinsonian rats.
J. Neurosci., April 5, 2006; 26(14): 3875 - 3884.
[Abstract] [Full Text] [PDF]
N. Gustafson, E. Gireesh-Dharmaraj, U. Czubayko, K. T. Blackwell, and D. Plenz
A Comparative Voltage and Current-Clamp Analysis of Feedback and Feedforward Synaptic Transmission in the Striatal Microcircuit In Vitro
J Neurophysiol, February 1, 2006; 95(2): 737 - 752.
[Abstract] [Full Text] [PDF]
J. H. Kotaleski, D. Plenz, and K. T. Blackwell
Using Potassium Currents to Solve Signal-to-Noise Problems in Inhibitory Feedforward Networks of the Striatum
J Neurophysiol, January 1, 2006; 95(1): 331 - 341.
[Abstract] [Full Text] [PDF]
H. Salgado, F. Tecuapetla, T. Perez-Rosello, A. Perez-Burgos, E. Perez-Garci, E. Galarraga, and J. Bargas
A Reconfiguration of CaV2 Ca2+ Channel Current and Its Dopaminergic D2 Modulation in Developing Neostriatal Neurons
J Neurophysiol, December 1, 2005; 94(6): 3771 - 3787.
[Abstract] [Full Text] [PDF]
N. Mallet, C. Le Moine, S. Charpier, and F. Gonon
Feedforward Inhibition of Projection Neurons by Fast-Spiking GABA Interneurons in the Rat Striatum In Vivo
J. Neurosci., April 13, 2005; 25(15): 3857 - 3869.
[Abstract] [Full Text] [PDF]
R. Lape and J. A. Dani
Complex Response to Afferent Excitatory Bursts by Nucleus Accumbens Medium Spiny Projection Neurons
J Neurophysiol, September 1, 2004; 92(3): 1276 - 1284.
[Abstract] [Full Text] [PDF]
S. J. Slaght, T. Paz, M. Chavez, J.-M. Deniau, S. Mahon, and S. Charpier
On the Activity of the Corticostriatal Networks during Spike-and-Wave Discharges in a Genetic Model of Absence Epilepsy
J. Neurosci., July 28, 2004; 24(30): 6816 - 6825.
[Abstract] [Full Text] [PDF]
J. M. Beggs and D. Plenz
Neuronal Avalanches Are Diverse and Precise Activity Patterns That Are Stable for Many Hours in Cortical Slice Cultures
J. Neurosci., June 2, 2004; 24(22): 5216 - 5229.
[Abstract] [Full Text] [PDF]
J. N. D. Kerr and D. Plenz
Action Potential Timing Determines Dendritic Calcium during Striatal Up-States
J. Neurosci., January 28, 2004; 24(4): 877 - 885.
[Abstract] [Full Text] [PDF]
J. M. Beggs and D. Plenz
Neuronal Avalanches in Neocortical Circuits
J. Neurosci., December 3, 2003; 23(35): 11167 - 11177.
[Abstract] [Full Text] [PDF]
R Vergara, C Rick, S Hernandez-Lopez, J A Laville, J N Guzman, E Galarraga, D J Surmeier, and J Bargas
Spontaneous voltage oscillations in striatal projection neurons in a rat corticostriatal slice
J. Physiol., November 15, 2003; 553(1): 169 - 182.
[Abstract] [Full Text] [PDF]
K. T. Blackwell, U. Czubayko, and D. Plenz
Quantitative Estimate of Synaptic Inputs to Striatal Neurons during Up and Down States In Vitro
J. Neurosci., October 8, 2003; 23(27): 9123 - 9132.
[Abstract] [Full Text] [PDF]
D. Centonze, C. Grande, A. Usiello, P. Gubellini, E. Erbs, A. B. Martin, A. Pisani, N. Tognazzi, G. Bernardi, R. Moratalla, et al.
Receptor Subtypes Involved in the Presynaptic and Postsynaptic Actions of Dopamine on Striatal Interneurons
J. Neurosci., July 16, 2003; 23(15): 6245 - 6254.
[Abstract] [Full Text] [PDF]
F. W. Hopf, M. G. Cascini, A. S. Gordon, I. Diamond, and A. Bonci
Cooperative Activation of Dopamine D1 and D2 Receptors Increases Spike Firing of Nucleus Accumbens Neurons via G-Protein {beta}{gamma} Subunits
J. Neurosci., June 15, 2003; 23(12): 5079 - 5087.
[Abstract] [Full Text] [PDF]
U. Czubayko and D. Plenz
Fast synaptic transmission between striatal spiny projection neurons
PNAS, November 26, 2002; 99(24): 15764 - 15769.
[Abstract] [Full Text] [PDF]
S. Ramanathan, J. J. Hanley, J.-M. Deniau, and J. P. Bolam
Synaptic Convergence of Motor and Somatosensory Cortical Afferents onto GABAergic Interneurons in the Rat Striatum
J. Neurosci., September 15, 2002; 22(18): 8158 - 8169.
[Abstract] [Full Text] [PDF]
A. R. West, H. Moore, and A. A. Grace
Direct Examination of Local Regulation of Membrane Activity in Striatal and Prefrontal Cortical Neurons in Vivo Using Simultaneous Intracellular Recording and Microdialysis
J. Pharmacol. Exp. Ther., June 1, 2002; 301(3): 867 - 877.
[Abstract] [Full Text] [PDF]
J. N. D. Kerr and D. Plenz
Dendritic Calcium Encodes Striatal Neuron Output during Up-States
J. Neurosci., March 1, 2002; 22(5): 1499 - 1512.
[Abstract] [Full Text] [PDF]
T. Koos and J. M. Tepper
Dual Cholinergic Control of Fast-Spiking Interneurons in the Neostriatum
J. Neurosci., January 15, 2002; 22(2): 529 - 535.
[Abstract] [Full Text] [PDF]
D. Centonze, E. Saulle, A. Pisani, G. Bernardi, and P. Calabresi
Adenosine-mediated inhibition of striatal GABAergic synaptic transmission during in vitro ischaemia
Brain, September 1, 2001; 124(9): 1855 - 1865.
[Abstract] [Full Text] [PDF]
M. D. Bevan, P. A. C. Booth, S. A. Eaton, and J. P. Bolam
Selective Innervation of Neostriatal Interneurons by a Subclass of Neuron in the Globus Pallidus of the Rat
J. Neurosci., November 15, 1998; 18(22): 9438 - 9452.
[Abstract] [Full Text] [PDF]
D. Plenz and S. T. Kitai
Regulation of the Nigrostriatal Pathway by Metabotropic Glutamate Receptors during Development
J. Neurosci., June 1, 1998; 18(11): 4133 - 4144.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|