Potassium channels control the interaction between active dendritic integration compartments in layer 5 cortical pyramidal neurons

Neuron

Volumn 79, Issue 3, 2013, Pages 516-529

  Harnett, Mark T ^a   Xu, Ning Long ^a   Magee, Jeffrey C ^a   Williams, Stephen R ^b  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

VOLTAGE GATED POTASSIUM CHANNEL;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN ELECTROPHYSIOLOGY; BRAIN SLICE; CONTROLLED STUDY; DENDRITE; IN VITRO STUDY; MALE; MOUSE; NEUROMODULATION; NONHUMAN; PATCH CLAMP; POTASSIUM TRANSPORT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PYRAMIDAL NERVE CELL; RAT; SENSORIMOTOR FUNCTION; SYNAPTIC TRANSMISSION;

ALKALOIDS; ANIMALS; BARIUM; CALCIUM; CALCIUM CHANNEL BLOCKERS; CALCIUM SIGNALING; DENDRITES; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; INDOLES; MALE; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNELS; PROBABILITY; PYRAMIDAL CELLS; QUINOLINES; RATS; RATS, WISTAR; SOMATOSENSORY CORTEX; TIME FACTORS; VALINE;

EID: 84881510670     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.06.005     Document Type: Article

References (45)

1. Atkinson S.E., Williams S.R. Postnatal development of dendritic synaptic integration in rat neocortical pyramidal neurons. J.Neurophysiol. 2009, 102:735-751.
2. Bekkers J.M. Distribution and activation of voltage-gated potassium channels in cell-attached and outside-out patches from large layer 5 cortical pyramidal neurons of the rat. J.Physiol. 2000, 525:611-620.
3. Bekkers J.M. Properties of voltage-gated potassium currents in nucleated patches from large layer 5 cortical pyramidal neurons of the rat. J.Physiol. 2000, 525:593-609.
4. Branco T., Clark B.A., Häusser M. Dendritic discrimination of temporal input sequences in cortical neurons. Science 2010, 329:1671-1675.
5. Cai X., Liang C.W., Muralidharan S., Kao J.P., Tang C.M., Thompson S.M. Unique roles of SK and Kv4.2 potassium channels in dendritic integration. Neuron 2004, 44:351-364.
6. Cauller L.J., Connors B.W. Synaptic physiology of horizontal afferents to layer I in slices of rat SI neocortex. J.Neurosci. 1994, 14:751-762.
7. Cauller L.J., Clancy B., Connors B.W. Backward cortical projections to primary somatosensory cortex in rats extend long horizontal axons in layer I. J.Comp. Neurol. 1998, 390:297-310.
8. de Kock C.P., Sakmann B. High frequency action potential bursts (>or= 100Hz) in L2/3 and L5B thick tufted neurons in anaesthetized and awake rat primary somatosensory cortex. J.Physiol. 2008, 586:3353-3364.
9. Engel D., Jonas P. Presynaptic action potential amplification by voltage-gated Na+ channels in hippocampal mossy fiber boutons. Neuron 2005, 45:405-417.
10. Gasparini S., Migliore M., Magee J.C. On the initiation and propagation of dendritic spikes in CA1 pyramidal neurons. J.Neurosci. 2004, 24:11046-11056.
11. Gilbert C.D., Sigman M. Brain states: top-down influences in sensory processing. Neuron 2007, 54:677-696.
12. Golding N.L., Jung H.Y., Mickus T., Spruston N. Dendritic calcium spike initiation and repolarization are controlled by distinct potassium channel subtypes in CA1 pyramidal neurons. J.Neurosci. 1999, 19:8789-8798.
13. Gregoriou G.G., Gotts S.J., Zhou H., Desimone R. High-frequency, long-range coupling between prefrontal and visual cortex during attention. Science 2009, 324:1207-1210.
14. Hoffman D.A., Johnston D. Downregulation of transient K+ channels in dendrites of hippocampal CA1 pyramidal neurons by activation of PKA and PKC. J.Neurosci. 1998, 18:3521-3528.
15. Hoffman D.A., Johnston D. Neuromodulation of dendritic action potentials. J.Neurophysiol. 1999, 81:408-411.
16. Hoffman D.A., Magee J.C., Colbert C.M., Johnston D. K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 1997, 387:869-875.
17. Hupe J.M., James A.C., Payne B.R., Lomber S.G., Girard P., Bullier J. Cortical feedback improves discrimination between figure and background by V1, V2 and V3 neurons. Nature 1998, 394:784-787.
18. Imaizumi Y., Giles W.R. Quinidine-induced inhibition of transient outward current in cardiac muscle. Am. J. Physiol. 1987, 253:H704-H708.
19. Kim H.G., Connors B.W. Apical dendrites of the neocortex: correlation between sodium- and calcium-dependent spiking and pyramidal cell morphology. J.Neurosci. 1993, 13:5301-5311.
20. Korngreen A., Sakmann B. Voltage-gated K+ channels in layer 5 neocortical pyramidal neurones from young rats: subtypes and gradients. J.Physiol. 2000, 525:621-639.
21. Larkman A.U. Dendritic morphology of pyramidal neurones of the visual cortex of the rat: III. Spine distributions. J.Comp. Neurol. 1991, 306:332-343.
22. Larkum M.E., Zhu J.J. Signaling of layer 1 and whisker-evoked Ca2+ and Na+ action potentials in distal and terminal dendrites of rat neocortical pyramidal neurons invitro and invivo. J.Neurosci. 2002, 22:6991-7005.
23. Larkum M.E., Zhu J.J., Sakmann B. A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 1999, 398:338-341.
24. Larkum M.E., Senn W., Lüscher H.R. Top-down dendritic input increases the gain of layer 5 pyramidal neurons. Cereb. Cortex 2004, 14:1059-1070.
25. Larkum M.E., Nevian T., Sandler M., Polsky A., Schiller J. Synaptic integration in tuft dendrites of layer 5 pyramidal neurons: a new unifying principle. Science 2009, 325:756-760.
26. Losonczy A., Magee J.C. Integrative properties of radial oblique dendrites in hippocampal CA1 pyramidal neurons. Neuron 2006, 50:291-307.
27. Losonczy A., Makara J.K., Magee J.C. Compartmentalized dendritic plasticity and input feature storage in neurons. Nature 2008, 452:436-441.
28. Matyas F., Sreenivasan V., Marbach F., Wacongne C., Barsy B., Mateo C., Aronoff R., Petersen C.C. Motor control by sensory cortex. Science 2010, 330:1240-1243.
29. Nicoll R.A., Malenka R.C., Kauer J.A. Functional comparison of neurotransmitter receptor subtypes in mammalian central nervous system. Physiol. Rev. 1990, 70:513-565.
30. O'Connor D.H., Peron S.P., Huber D., Svoboda K. Neural activity in barrel cortex underlying vibrissa-based object localization in mice. Neuron 2010, 67:1048-1061.
31. Oberlaender M., de Kock C.P., Bruno R.M., Ramirez A., Meyer H.S., Dercksen V.J., Helmstaedter M., Sakmann B. Cell type-specific three-dimensional structure of thalamocortical circuits in a column of rat vibrissal cortex. Cereb. Cortex 2012, 22:2375-2391.
32. Petreanu L., Mao T., Sternson S.M., Svoboda K. The subcellular organization of neocortical excitatory connections. Nature 2009, 457:1142-1145.
33. Rall W. Theoretical significance of dendritic trees for neuronal input-output relations. Neural Theory and Modeling 1964, 73-94. Stanford Univ. Press, Palo Alto, CA. R.F. Reiss (Ed.).
34. Schaefer A.T., Helmstaedter M., Schmitt A.C., Bar-Yehuda D., Almog M., Ben-Porat H., Sakmann B., Korngreen A. Dendritic voltage-gated K+ conductance gradient in pyramidal neurones of neocortical layer 5B from rats. J.Physiol. 2007, 579:737-752.
35. Schiller J., Schiller Y., Stuart G., Sakmann B. Calcium action potentials restricted to distal apical dendrites of rat neocortical pyramidal neurons. J.Physiol. 1997, 505:605-616.
36. Schiller J., Major G., Koester H.J., Schiller Y. NMDA spikes in basal dendrites of cortical pyramidal neurons. Nature 2000, 404:285-289.
37. Takahashi H., Magee J.C. Pathway interactions and synaptic plasticity in the dendritic tuft regions of CA1 pyramidal neurons. Neuron 2009, 62:102-111.
38. Vetter P., Roth A., Häusser M. Propagation of action potentials in dendrites depends on dendritic morphology. J.Neurophysiol. 2001, 85:926-937.
39. Williams S.R. Spatial compartmentalization and functional impact of conductance in pyramidal neurons. Nat. Neurosci. 2004, 7:961-967.
40. Williams S.R. Encoding and decoding of dendritic excitation during active states in pyramidal neurons. J.Neurosci. 2005, 25:5894-5902.
41. Williams S.R., Stuart G.J. Dependence of EPSP efficacy on synapse location in neocortical pyramidal neurons. Science 2002, 295:1907-1910.
42. Williams S.R., Atkinson S.E. Pathway-specific use-dependent dynamics of excitatory synaptic transmission in rat intracortical circuits. J.Physiol. 2007, 585:759-777.
43. Wimmer V.C., Bruno R.M., de Kock C.P., Kuner T., Sakmann B. Dimensions of a projection column and architecture of VPM and POm axons in rat vibrissal cortex. Cereb. Cortex 2010, 20:2265-2276.
44. Xu N.-L., Harnett M.T., Williams S.R., Huber D., O'Connor D.H., Svoboda K., Magee J.C. Nonlinear dendritic integration of sensory and motor pathways produces an object localization signal. Nature 2012, 492:247-251.
45. Yue L., Feng J.L., Wang Z., Nattel S. Effects of ambasilide, quinidine, flecainide and verapamil on ultra-rapid delayed rectifier potassium currents in canine atrial myocytes. Cardiovasc. Res. 2000, 46:151-161.