UP States Protect Ongoing Cortical Activity from Thalamic Inputs

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2008 Dec 19

PMID 19092994

Citations 35

Authors

Brendon O Watson

Jason N MacLean

Rafael Yuste

Affiliations

Soon will be listed here.

Abstract

Cortical neurons in vitro and in vivo fluctuate spontaneously between two stable membrane potentials: a depolarized UP state and a hyperpolarized DOWN state. UP states temporally correspond with multineuronal firing sequences which may be important for information processing. To examine how thalamic inputs interact with ongoing cortical UP state activity, we used calcium imaging and targeted whole-cell recordings of activated neurons in thalamocortical slices of mouse somatosensory cortex. Whereas thalamic stimulation during DOWN states generated multineuronal, synchronized UP states, identical stimulation during UP states had no effect on the subthreshold membrane dynamics of the vast majority of cells or on ongoing multineuronal temporal patterns. Both thalamocortical and corticocortical PSPs were significantly reduced and neuronal input resistance was significantly decreased during cortical UP states -- mechanistically consistent with UP state insensitivity. Our results demonstrate that cortical dynamics during UP states are insensitive to thalamic inputs.

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References

Kali S, Dayan P . Off-line replay maintains declarative memories in a model of hippocampal-neocortical interactions. Nat Neurosci. 2004; 7(3):286-94. DOI: 10.1038/nn1202. View

Beierlein M, Fall C, Rinzel J, Yuste R . Thalamocortical bursts trigger recurrent activity in neocortical networks: layer 4 as a frequency-dependent gate. J Neurosci. 2002; 22(22):9885-94. PMC: 6757840. View

Agmon A, Connors B . Thalamocortical responses of mouse somatosensory (barrel) cortex in vitro. Neuroscience. 1991; 41(2-3):365-79. DOI: 10.1016/0306-4522(91)90333-j. View

Ikegaya Y, Aaron G, Cossart R, Aronov D, Lampl I, Ferster D . Synfire chains and cortical songs: temporal modules of cortical activity. Science. 2004; 304(5670):559-64. DOI: 10.1126/science.1093173. View

Bruno R, Sakmann B . Cortex is driven by weak but synchronously active thalamocortical synapses. Science. 2006; 312(5780):1622-7. DOI: 10.1126/science.1124593. View

Hasenstaub A, Sachdev R, McCormick D . State changes rapidly modulate cortical neuronal responsiveness. J Neurosci. 2007; 27(36):9607-22. PMC: 6672966. DOI: 10.1523/JNEUROSCI.2184-07.2007. View

Petersen C, Hahn T, Mehta M, Grinvald A, Sakmann B . Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex. Proc Natl Acad Sci U S A. 2003; 100(23):13638-43. PMC: 263866. DOI: 10.1073/pnas.2235811100. View

Cossart R, Aronov D, Yuste R . Attractor dynamics of network UP states in the neocortex. Nature. 2003; 423(6937):283-8. DOI: 10.1038/nature01614. View

No R, Condouris G . DECREMENTAL CONDUCTION IN PERIPHERAL NERVE. INTEGRATION OF STIMULI IN THE NEURON. Proc Natl Acad Sci U S A. 1959; 45(4):592-617. PMC: 222605. DOI: 10.1073/pnas.45.4.592. View

10.

MacLean J, Watson B, Aaron G, Yuste R . Internal dynamics determine the cortical response to thalamic stimulation. Neuron. 2005; 48(5):811-23. DOI: 10.1016/j.neuron.2005.09.035. View

11.

Luczak A, Bartho P, Marguet S, Buzsaki G, Harris K . Sequential structure of neocortical spontaneous activity in vivo. Proc Natl Acad Sci U S A. 2006; 104(1):347-52. PMC: 1765463. DOI: 10.1073/pnas.0605643104. View

12.

Fox M, Snyder A, Vincent J, Raichle M . Intrinsic fluctuations within cortical systems account for intertrial variability in human behavior. Neuron. 2007; 56(1):171-84. DOI: 10.1016/j.neuron.2007.08.023. View

13.

Destexhe A, Rudolph M, Pare D . The high-conductance state of neocortical neurons in vivo. Nat Rev Neurosci. 2003; 4(9):739-51. DOI: 10.1038/nrn1198. View

14.

Araya R, Jiang J, Eisenthal K, Yuste R . The spine neck filters membrane potentials. Proc Natl Acad Sci U S A. 2006; 103(47):17961-6. PMC: 1693855. DOI: 10.1073/pnas.0608755103. View

15.

Shu Y, Hasenstaub A, McCormick D . Turning on and off recurrent balanced cortical activity. Nature. 2003; 423(6937):288-93. DOI: 10.1038/nature01616. View

16.

Yuste R, Katz L . Control of postsynaptic Ca2+ influx in developing neocortex by excitatory and inhibitory neurotransmitters. Neuron. 1991; 6(3):333-44. DOI: 10.1016/0896-6273(91)90243-s. View

17.

Wilson M, McNaughton B . Reactivation of hippocampal ensemble memories during sleep. Science. 1994; 265(5172):676-9. DOI: 10.1126/science.8036517. View

18.

MacLean J, Fenstermaker V, Watson B, Yuste R . A visual thalamocortical slice. Nat Methods. 2006; 3(2):129-34. DOI: 10.1038/nmeth849. View

19.

Gonzalez-Burgos G, Barrionuevo G . Voltage-gated sodium channels shape subthreshold EPSPs in layer 5 pyramidal neurons from rat prefrontal cortex. J Neurophysiol. 2001; 86(4):1671-84. DOI: 10.1152/jn.2001.86.4.1671. View

20.

Smetters D, Majewska A, Yuste R . Detecting action potentials in neuronal populations with calcium imaging. Methods. 1999; 18(2):215-21. DOI: 10.1006/meth.1999.0774. View