Electrophysiological properties of genetically identified subtypes of layer 5 neocortical pyramidal neurons: Ca2+ dependence and differential modulation by norepinephrine

Journal of Neurophysiology

Volumn 113, Issue 7, 2015, Pages 2014-2032

  Guan, Dongxu ^a   Armstrong, William E ^a   Foehring, Robert C ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Afterhyperpolarization; Bacterial artificial chromosome mice; Repetitive firing

Indexed keywords

CALCIUM; CALCIUM ACTIVATED POTASSIUM CHANNEL; ENHANCED GREEN FLUORESCENT PROTEIN; NORADRENALIN; TRANSCRIPTION FACTOR ER81;

AFTERHYPERPOLARIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; BRAIN SLICE; CELL FUNCTION; CELL SIZE; CELL STRUCTURE; CELLS BY BODY ANATOMY; CONTROLLED STUDY; DIRECT CURRENT; ELECTROPHYSIOLOGY; GENE EXPRESSION; GENETIC IDENTIFICATION; MOUSE; NEOCORTEX; NONHUMAN; PRIMARY SOMATOSENSORY CORTEX; PRIORITY JOURNAL; PROTEIN FUNCTION; PYRAMIDAL NERVE CELL; RECEPTIVE FIELD; SOMATOSENSORY CORTEX; SPIKE WAVE; ANIMAL; CYTOLOGY; DRUG EFFECTS; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; CALCIUM; MICE; MICE, TRANSGENIC; NEOCORTEX; NOREPINEPHRINE; ORGAN CULTURE TECHNIQUES; PYRAMIDAL CELLS;

EID: 84926367895     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00524.2014     Document Type: Article

References (102)

1. Abel HJ, Lee J, Callaway JC, Foehring RC. Relationships between action potentials, afterhyperpolarizations, and calcium signaling in layer II/III neocortical pyramidal neurons. J Neurophysiol 91: 324-335, 2004.
2. Agmon A, Connors BW. Correlation between intrinsic firing patterns and thalamocortical synaptic responses of neurons in mouse barrel cortex. J Neurosci 12: 319-329, 1992.
3. Akintunde A, Buxton DF. Origins and collateralization of corticospinal, corticopontine, corticorubral and corticostriatal tracts: a multiple retrograde fluorescent tracing study. Brain Res 586: 208-218, 1992.
4. Andrade R, Foehring RC, Tzingounis AV. The calcium-activated slow AHP: cutting through the Gordian knot. Front Mol Neurosci 6: 47, 2012.
5. Arlotta P, Molyneaux BJ, Chen J, Inoue J, Kominami R, Macklis JD. Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo. Neuron 45: 207-221, 2005.
6. Arber S, Ladle DR, Lin JH, Frank E, Jessell TM. ETS gene Er81 controls the formation of functional connections between group Ia sensory afferents and motor neurons. Cell 101: 485-498, 2000.
7. Aston-Jones G, Rajkowski J, Cohen J. Role of locus coeruleus in attention and behavioral flexibility. Biol Psychiatry 46: 1309-1320, 1999.
8. Avesar D, Guledge AT. Selective serotonergic excitation of callosal projection neurons. Front Neural Circuits 6: 12, 2012.
9. Bean BP. The action potential in mammalian central neurons. Nat Rev Neurosci 8: 451-465, 2007.
10. Berridge CW, Waterhouse BD. The locus coeruleus-noradrenergic system: Modulation of behavioral state and state-dependent cognitive processes. Brain Res Rev 42: 33-84, 2003.
11. Breton JD, Stuart GJ. Loss of sensory input increases the intrinsic excitability of layer 5 pyramidal neurons in rat barrel cortex. J Physiol 587: 5107-5119, 2009.
12. Brown SP, Hestrin S. Intracortical circuits of pyramidal neurons reflect their long-range axonal targets. Nature 457: 1133-1136, 2009.
13. Catsman-Berrevoets CE, Lemon RN, Verburgh CA, Bentivoglio M, Kuypers HG. Absence of callosal collaterals derived from rat corticospinal neurons. A study using fluorescent retrograde tracing and electrophysiolog-ical techniques. Exp Brain Res 39: 433-440, 1980.
14. Chance F, Abbott L, Reyes A. Gain modulation from background synaptic input. Neuron 35: 773-782, 2002.
15. Chagnac-Amitai Y, Luhmann HJ, Prince DA. Burst generating and regular spiking layer 5 pyramidal neurons of rat neocortex have different morphological features. J Comp Neurol 296: 598-613, 1990.
16. Christophe E, Doerflinger N, Lavery DJ, Molnar Z, Charpak S, Audinat E. Two populations of layer V pyramidal cells of the mouse neocortex: development and sensitivity to anesthetics. J Neurophysiol 94: 3357-3367, 2005.
17. Connors BW, Gutnick MJ, Prince DA. Electrophysiological properties of neocortical neurons in vitro. J Neurophysiol 48: 1302-1320, 1982.
18. Cowan RL, Wilson CJ. Spontaneous firing patterns and axonal projections of single corticostriatal neurons in the rat medial agranular cortex. J Neurophysiol 71: 17-32, 1994.
19. Dembrow NC, Chitwood D, Johnston RA. Projection-specific neuromodulation of medial prefrontal cortex neurons. J Neurosci 30: 16922-16937, 2010.
20. Dodt HU, Zieglgansberger W. Visualizing unstained neurons in living brain slices by infrared DIC-videomicroscopy. Brain Res 537: 333-336, 1990.
21. Doyle JP, Dougherty JD, Heiman M, Schmidt EF, Stevens TR, Ma G, Bupp S, Shrestha P, Shah RD, Doughty ML, Gong S, Greengard P, Heintz N. Application of a translational profiling approach for the comparative analysis of CNS cell types. Cell 135: 749-762, 2008.
22. Etherington SJ, Williams SR. Postnatal development of intrinsic and synaptic properties transforms signaling in the layer 5 excitatory neural network of the visual cortex. J Neurosci 31: 9526-9537, 2011.
23. Fakler B, Adelman JP. Control of K(Ca) channels by calcium nano/microdomains. Neuron 59: 873-881, 2008.
24. Foehring RC, Schwindt PC, Crill WE. Norepinephrine selectively reduces slow Ca2+-and Na+ mediated K+ currents in cat neocortical neurons. J Neurophysiol 61: 245-256, 1989.
25. Franceschetti S, Sancini G, Panzica F, Radici C, Avanzini G. Postnatal differentiation of firing properties and morphological characteristics in layer pyramidal neurons of the sensorimotor cortex. Neuroscience 83: 1013-1024, 1998.
26. Gee S, Ellwood I, Patel T, Luongo F, Deisseroth K, Sohal VS. Synaptic activity unmasks dopamine D2 receptor modulation of a specific class of layer V pyramidal neurons in prefrontal cortex. J Neurosci 32: 4959-4971, 2012.
27. Gong S, Yang XW, Li C, Heintz N. Highly efficient modification of bacterial artificial chromosomes (BACs) using novel shuttle vectors containing the R6Kgamma origin of replication. Genome Res 12: 1992-1998, 2002.
28. Gong S, Zheng C, Doughty ML, Losos K, Didkovsky N, Schambra UB, Nowak NJ, Joyner A, Leblanc G, Hatten ME, Heintz N. A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425: 917-925, 2003.
29. Gong S, Doughty M, Harbaugh CR, Cummins A, Hatten ME, Heintz N, Gerfen CR. Targeting Cre recombinase to specific neuron populations with bacterial artificial chromosome constructs. J Neurosci 27: 9817-9823, 2007.
30. Greig LC, Woodworth MB, Galazo MJ, Padmanobhan H, Macklis JD. Molecular logic of neocortical projection neuron specification, development, and diversity. Nat Rev Neurosci 14: 755-769, 2013.
31. Groh A, Hanno Meyer S, Eric F, Schmidt, Heintz N, Sakmann B, Krieger P. Cell-type specific properties of pyramidal neurons in neocortex underlying a layout that is modifiable depending on the cortical area. Cereb Cortex 20: 826-836, 2010.
32. Guan D, Armstrong WE, Foehring RC. Kv2 channels regulate firing rate in pyramidal neurons from rat sensorimotor cortex. J Physiol 591: 4807-4825, 2013.
33. Gulledge AT, Dasari S, Onoue K, Stephens EK, Hasse JM, Avesar D. A sodium-pump-mediated afterhyperpolarization in pyramidal neurons. J Neu-rosci 33:13025-13041, 2013.
34. Hattox AM, Nelson SB. Layer V neurons in mouse cortex projecting to different targets have distinct physiological properties. J Neurophysiol 98: 3330-3340, 2007.
35. Hedrick T, Waters J. Effect of temperature on spiking patterns of neocortical layer 2/3 and layer 6 pyramidal neurons. Front Neural Circuits 6: 28, 2012.
36. Hevner RF, Daza RA, Rubenstein JL, Stunnenberg H, Olavarria JF, Englund C. Beyond laminar fate: toward a molecular classification of cortical projection/pyramidal neurons. Dev Neurosci 25: 139-151, 2003.
37. Higgs MH, Slee SJ, Spain WJ. Diversity of gain modulation by noise in neocortical neurons: regulation by the slow afterhyperpolarization conductance. J Neurosci 26: 8787-8799, 2006.
38. Jones SL, Stuart GJ. Different calcium sources control somatic versus dendritic SK channel activation during action potentials. J Neurosci 33: 19396-19405, 2013.
39. Kaczorowski CC, Disterhoft J, Spruston N. Stability and plasticity of intrinsic membrane properties in hippocampal CA1 pyramidal neurons: effects of internal anions. J Physiol 578: 799-818, 2007.
40. Kasper EM, Larkman AU, Lubke J, Blakemore C. Pyramidal neurons in layer 5 of the rat visual cortex. I. Correlation among cell morphology, intrinsic electrophysiological properties, and axon targets. J Comp Neurol 339: 459-474, 1994.
41. Kepecs A, Wang XJ, Lisman J. Bursting neurons signal input slope. J Neurosci 22: 9053-9062, 2002.
42. Kress GJ, Yamawaki N, Wokosin DL, Wickersham IR, Shepherd GM, Surmeier DJ. Convergent cortical innervation of striatal projection neurons. Nat Neurosci 16: 665-667, 2013.
43. Larkman A, Mason A. Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. I. Establishment of cell classes. J Neurosci 10: 1407-1414, 1990.
44. Larkum ME, Waters J, Sakmann B, Helmchen F. Dendritic spikes in apical dendrites of neocortical layer 2/3 pyramidal neurons. J Neurosci 27: 89999008, 2007.
45. Larkum ME, Senn W, Luscher HR. Top-down dendritic input increases the gain of layer 5 pyramidal neurons. Cereb Cortex 14: 1059-1070, 2004.
46. Larkum ME, Zhu JJ, Sakmann B. A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 398: 338-341, 1999.
47. Larkum ME, Zhu JJ, Sakmann B. Dendritic mechanisms underlying the coupling of the dendritic with the axonal action potential initiation zone of adult rat layer 5 pyramidal neurons. J Physiol 533: 447-466, 2001.
48. Le Be JV, Silberberg G, Wang Y, Markram H. Morphological, electro-physiological, and synaptic properties of corticocallosal pyramidal cells in the neonatal rat neocortex. Cereb Cortex 17: 2204-2213, 2007.
49. Lisman JE. Bursts as a unit of neural information: making unreliable synapses reliable. Trends Neurosci 20: 38-43, 1997.
50. Lorenzon NM, Foehring RC. Relationships of afterhyperpolarizations to repetitive firing in human neocortical neurons in vitro. J Neurophysiol 67: 350-363, 1992.
51. Lorenzon NM, Foehring RC. The ontogeny of repetitive firing its modulation by norepinephrine in rat neocortical neurons. Dev Brain Res 73: 213-223, 1993.
52. Lorenzon NM, Foehring RC. Alterations in intracellular calcium chelation reproduce developmental differences in repetitive firing and afterhyperpolarizations in rat neocortical neurons. Brain Res Dev Brain Res 84: 192-203, 1995.
53. Madison DV, Nicoll RA. Noradrenaline blocks accommodation of pyramidal cell discharge in the hippocampus. Nature 299: 636-638, 1982.
54. Markram H, Lubke J, Frotscher M, Roth A, Sakmann B. Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J Physiol 500: 409-440, 1997.
55. Mason A, Larkman A. Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. II. Electrophysiology. J Neurosci 10: 1415-1428, 1990.
56. McAdams CJ, Maunsell JHR. Effects of attention on orientation-tuning functions of single neurons in macaque cortical area V4. J Neurosci 19: 431-441, 1999.
57. McCormick DA, Connors BW, Lighthall JW, Prince DA. Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol 54: 782-806, 1985.
58. Miller MN, Okaty BW, Nelson SB. Region-specific spike-frequency acceleration in layer 5 pyramidal neurons mediated by Kv1 subunits. J Neurosci 28: 13716-13726, 2008.
59. Mitchell BD, Macklis JD. Large-scale maintenance of dual projections by callosal and frontal cortical projection neurons in adult mice. J Comp Neurol 482: 17-32, 2005.
60. Molnar Z, Cheung AF. Towards the classification of subpopulations of layer pyramidal projection neurons. Neurosci Res 55: 105-115, 2006.
61. Molyneaux BJ, Arlotta P, Fame RM, MacDonald JL, MacQuarrie KL, Macklis JD. Novel subtype-specific genes identify distinct subpopulations of callosal projection neurons. J Neurosci 29: 12343-12354, 2009.
62. Morishima M, Morita K, Kubota Y, Kawaguchi Y. Highly differentiated projection-specific cortical subnetworks. J Neurosci 31: 10380-10391, 2011.
63. Pineda JC, Waters R, Foehring RC. Specificity in the interaction of Ca2+ channel types with Ca2+-dependent AHPs and firing behavior in neocortical pyramidal neurons. J Neurophysiol 79: 2522-2534, 1998.
64. Reiner A, Jiao Y, Del Mar N, Laverghetta AV, Lei WL. Differential morphology of pyramidal tract-type and intratelencephalically projecting-type corticostriatal neurons and their intrastriatal terminals in rats. J Comp Neurol 457: 420-440, 2003.
65. Reiner A, Hart NM, Lei W, Deng Y. Corticostriatal projection neurons— dichotomous types and dichotomous functions. Front Neuroanat 4: 142, 2010.
66. Rumberger A, Schmidt M, Lohmann H, Hoffmann KP. Correlation of electrophysiology, morphology, and functions in corticotectal and cortico-pretectal projection neurons in rat visual cortex. Exp Brain Res 119: 375-390, 1998.
67. Salinas E, Thier P. Gain modulation: a major computation principle of the central nervous system. Neuron 27: 15-21, 2000.
68. Schmidt EF, Warner-Schmidt JL, Otopalik BG, Pickett SB, Greengard P, Heintz N. Identification of the cortical neurons that mediate antidepressant responses. Cell 149: 1152-1163, 2012.
69. Schubert D, Kotter R, Luhmann HJ, Staiger JF. Morphology, electrophysiology and functional input connectivity of pyramidal neurons characterizes a genuine layer Va in the primary somatosensory cortex. Cereb Cortex 16: 223-236, 2006.
70. Schwindt P, O’Brien JA, Crill W. Quantitative analysis of pyramidal neurons from layer 5 of rat sensorimotor cortex. J Neurophysiol 77: 2484-2498, 1997.
71. Schwindt PC, Spain WJ, Crill WE. Calcium-dependent potassium currents in neurons from cat sensorimotor cortex. J Neurophysiol 67: 216-226, 1992a.
72. Schwindt PC, Spain WJ, Crill WE. Effects of intracellular calcium chelation on voltage-dependent and calcium-dependent currents in cat neocortical neurons. Neuroscience 47: 571-578, 1992b.
73. Schwindt PC, Spain WJ, Foehring RC, Chubb MC, Crill WE. Slow conductances in neurons from cat sensorimotor cortex in vitro: Their modulation by neurotransmitters and their role in slow excitability changes. J Neurophysiol 59: 450-467, 1988a.
74. Schwindt PC, Spain WJ, Foehring RC, Stafstrom CE, Chubb MC, Crill WE. Multiple potassium conductances and their functions in neurons from cat sensorimotor cortex in vitro. J Neurophysiol 59: 424-449, 1988b.
75. Schwindt PC, Spain WJ, Crill WE. Influence of anomalous rectifier activation on afterhyperpolarizations of neurons from cat sensorimotor cortex in vitro. J Neurophysiol 59: 468-481, 1988c.
76. Sharifullina E. Structure and Function Studies in Layer 5 Pyramidal Neurons of the Mouse Vibrissal Cortex. PhD Dissertation. Fakultat fur Medizin der Technischen Universitat Munchen, 2011.
77. Shepherd GM. Corticostriatal connectivity and its role in disease. Nat Rev Neurosci 14: 278-291, 2013.
78. Sheets PL, Suter BA, Kiritani T, Chan CS, Surmeier DJ, Shepherd GM. Corticospinal-specific HCN expression in mouse motor cortex: I(h)-depen-dent synaptic integration as a candidate microcircuit mechanism involved in motor control. J Neurophysiol 106: 2216-2231, 2011.
79. Solomon JS, Doyle JF, Burkhalter A, Nerbonne JM. Differential expression of hyperpolarization-activated currents reveals distinct classes of visual cortical projection neurons. J Neurosci 13: 5082-5091, 1993.
80. Spain WJ, Schwindt PC, Crill WE. Post-inhibitory excitation and inhibition in layer V pyramidal neurones from cat sensorimotor cortex. J Physiol 434: 609-626, 1991.
81. Stenman J, Toresson H, Campbell K. Identification of two distinct progenitor populations in the lateral ganglionic eminence: implications for striatal and olfactory bulb neurogenesis. J Neurosci 23: 167-174, 2003.
82. Steriade M, McCormick DA, Sejnowski TJ. Thalamocortical oscillations in the sleeping and aroused brain. Science 262: 679-685, 1993.
83. Stern EA, Kincaid AE, Wilson CJ. Spontaneous subthreshold membrane potential fluctuations and action potential variability of rat corticostriatal and striatal neurons in vivo. J Neurophysiol 77: 1697-1715, 1997.
84. Storm JF. Action potential repolarization and a fast after-hyperpolarization in rat hippocampal pyramidal cells. J Physiol 385: 733-759, 1987.
85. Storm JF. An after-hyperpolarization of medium duration in rat hippocampal pyramidal cells. J Physiol 409: 171-190, 1989.
86. Stuart GJ, Dodt HU, Sakmann B. Patch-clamp recordings from the soma and dendrites of neurons in brain slices using infrared video microscopy. PflUgers Arch 423: 511-518, 1993.
87. Sugino K, Hempel CM, Miller MN, Hattox AM, Shapiro P, Wu C, Huang ZJ, Nelson SB. Molecular taxonomy of major neuronal classes in the adult mouse forebrain. Nat Neurosci 9: 99-107, 2006.
88. Sun X, Gu XQ, Haddad GG. Calcium influx via L-and N-type calcium channels activates a transient large-conductance Ca2+-activated K+ current in mouse neocortical pyramidal neurons. J Neurosci 23: 3639-3648, 2003.
89. Suter BA, Migliore M, Shepherd GM. Intrinsic electrophysiology of mouse corticospinal neurons: a class-specific triad of spike-related properties. Cereb Cortex 23: 1965-1977, 2013.
90. Toledo-Rodriguez M, Blumenfeld B, Wu C, Luo J, Attali B, Goodman P, Markram H. Correlation maps allow neuronal electrical properties to be predicted from single-cell gene expression profiles in rat neocortex. Cereb Cortex 14: 1310-1327, 2004.
91. Traub RD, Buhl EH, Gloveli T, Whittington MA. Fast rhythmic bursting can be induced in layer 2/3 cortical neurons by enhancing persistent Na+ conductance or by blocking BK channels. J Neurophysiol 89: 909-921, 2003.
92. Treue S, Martinez-Trujillo JC. Feature-based attention influences motion processing gain in macaque visual cortex. Nature 399: 575-579, 1999.
93. Tsiola A, Hamzei-Sichani F, Peterlin Z, Yuste R. Quantitative morphologic classification of layer 5 neurons from mouse primary visual cortex. J Comp Neurol 461: 415-428, 2003.
94. Tukey JW. Exploratory Data Analysis. Reading, PA: Addsion-Wesley, 1977.
95. Ueta Y, Hirai Y, Otsuka T, Kawaguchi Y. Direction-and distance-dependent interareal connectivity of pyramidal cell subpopulations in the rat frontal cortex. Front Neur Circuits 7: 164, 2013.
96. Wang Z, McCormick DA. Control of firing mode of corticotectal and corticopontine layer V burst-generating neurons by norepinephrine, acetylcholine, and 1S,3R-ACPD. JNeurosci 13: 2199-2216, 1993.
97. Wang M, Ramos BP, Paspalas CD, Shu Y, Simen A, Duque A, Vijay-raghavan S, Brennan A, Dudley A, Nou E, Mazer JA, McCormick DA, Arnsten AF. Alpha2A-adrenoceptors strengthen working memory networks by inhibiting cAMP-HCN channel signaling in prefrontal cortex. Cell 129: 397-410, 2007.
98. Watakabe A, Ichinohe N, Ohsawa S, Hashikawa T, Komatsu Y, Rockland KS, Yamamori T. Comparative analysis of layer-specific genes in mammalian neocortex. Cereb Cortex 17: 1918-1933, 2007.
99. Waterhouse BD, Mouradian R, Sessler FM, Lin RC. Differential modulatory effects of norepinephrine on synaptically driven responses of layer V barrel field cortical neurons. Brain Res 868: 39-47, 2000.
100. Wilson CJ. Morphology and synaptic connections of crossed corticostriatal neurons in the rat. J Comp Neurol 263: 567-580, 1987.
101. Wise SP, Jones EG. The organization and postnatal development of the commissural projection of the rat somatic sensory cortex. J Comp Neurol 168: 313-343, 1976.
102. Yoneshima H, Yamasaki S, Voelker CC, Molnar Z, Christophe E, Audinat E, Takemoto M, Nishiwaki M, Tsuji S, Fujita I, Yamamoto N. Er81 is expressed in a subpopulation of layer 5 neurons in rodent and primate neocortices. Neuroscience 137: 401-412, 2006.