Display options
Share it on

Front Cell Neurosci. 2015 Dec 10;9:471. doi: 10.3389/fncel.2015.00471. eCollection 2015.

Control of Phasic Firing by a Background Leak Current in Avian Forebrain Auditory Neurons.

Frontiers in cellular neuroscience

André A Dagostin, Peter V Lovell, Markus M Hilscher, Claudio V Mello, Ricardo M Leão

Affiliations

  1. Department of Physiology, School of Medicine of Ribeirão Preto, University of São Paulo Ribeirão Preto, Brazil.
  2. Department of Behavioral Neuroscience, Oregon Health and Science University, Portland OR, USA.
  3. Brain Institute, Federal University of Rio Grande do Norte Natal, Brazil ; Institute for Analysis and Scientific Computing, Vienna University of Technology Vienna, Austria.

PMID: 26696830 PMCID: PMC4674572 DOI: 10.3389/fncel.2015.00471

Abstract

Central neurons express a variety of neuronal types and ion channels that promote firing heterogeneity among their distinct neuronal populations. Action potential (AP) phasic firing, produced by low-threshold voltage-activated potassium currents (VAKCs), is commonly observed in mammalian brainstem neurons involved in the processing of temporal properties of the acoustic information. The avian caudomedial nidopallium (NCM) is an auditory area analogous to portions of the mammalian auditory cortex that is involved in the perceptual discrimination and memorization of birdsong and shows complex responses to auditory stimuli We performed in vitro whole-cell patch-clamp recordings in brain slices from adult zebra finches (Taeniopygia guttata) and observed that half of NCM neurons fire APs phasically in response to membrane depolarizations, while the rest fire transiently or tonically. Phasic neurons fired APs faster and with more temporal precision than tonic and transient neurons. These neurons had similar membrane resting potentials, but phasic neurons had lower membrane input resistance and time constant. Surprisingly phasic neurons did not express low-threshold VAKCs, which curtailed firing in phasic mammalian brainstem neurons, having similar VAKCs to other NCM neurons. The phasic firing was determined not by VAKCs, but by the potassium background leak conductances, which was more prominently expressed in phasic neurons, a result corroborated by pharmacological, dynamic-clamp, and modeling experiments. These results reveal a new role for leak currents in generating firing diversity in central neurons.

Keywords: action potentials; birdsong; leak current; potassium currents; zebra finch

References

  1. Nature. 1984 May 31-Jun 6;309(5967):453-6 - PubMed
  2. J Neurophysiol. 2006 Sep;96(3):1203-14 - PubMed
  3. J Comp Neurol. 1996 Mar 4;366(2):320-34 - PubMed
  4. Science. 1988 Dec 23;242(4886):1654-64 - PubMed
  5. J Comp Neurol. 1998 Jun 1;395(2):137-60 - PubMed
  6. J Neurophysiol. 2005 Dec;94(6):3698-707 - PubMed
  7. J Neurosci. 1999 Apr 15;19(8):2897-905 - PubMed
  8. J Physiol. 1952 Apr;116(4):449-72 - PubMed
  9. Curr Med Chem. 2007;14(13):1437-57 - PubMed
  10. J Neurosci. 1994 Sep;14(9):5352-64 - PubMed
  11. Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):6818-22 - PubMed
  12. Nat Rev Neurosci. 2008 Jul;9(7):557-68 - PubMed
  13. PLoS Biol. 2008 Mar 18;6(3):e62 - PubMed
  14. Trends Neurosci. 2004 Apr;27(4):210-7 - PubMed
  15. J Neurophysiol. 2007 Oct;98(4):1953-64 - PubMed
  16. Front Neural Circuits. 2013 Jul 23;7:120 - PubMed
  17. J Neurosci. 1991 Sep;11(9):2865-80 - PubMed
  18. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2012 Sep;198(9):705-16 - PubMed
  19. Nat Neurosci. 2008 May;11(5):579-86 - PubMed
  20. Mol Cell Neurosci. 2004 Dec;27(4):343-69 - PubMed
  21. J Physiol. 1999 Jan 1;514 ( Pt 1):125-38 - PubMed
  22. J Neurophysiol. 2006 Jan;95(1):76-87 - PubMed
  23. Physiol Rev. 2010 Jan;90(1):291-366 - PubMed
  24. J Physiol. 2007 Jan 15;578(Pt 2):377-85 - PubMed
  25. J Neurosci. 1995 Dec;15(12):8011-22 - PubMed
  26. J Neurosci. 1994 Nov;14(11 Pt 1):6652-66 - PubMed
  27. BMC Genomics. 2013 Jul 11;14:470 - PubMed
  28. Bioessays. 2011 May;33(5):377-85 - PubMed
  29. J Neurophysiol. 2008 Jul;100(1):441-55 - PubMed
  30. Methods Enzymol. 1992;207:123-31 - PubMed
  31. Annu Rev Physiol. 1999;61:497-519 - PubMed
  32. J Neurophysiol. 2001 Feb;85(2):523-38 - PubMed
  33. Pharmacol Rev. 2005 Dec;57(4):473-508 - PubMed
  34. J Neurophysiol. 2003 Jun;89(6):3097-113 - PubMed
  35. Physiol Rev. 2009 Jul;89(3):847-85 - PubMed
  36. Hear Res. 2008 Oct;244(1-2):98-106 - PubMed
  37. Nat Rev Neurosci. 2006 May;7(5):347-57 - PubMed
  38. Curr Biol. 2007 May 1;17(9):789-93 - PubMed
  39. J Physiol. 2005 Apr 1;564(Pt 1):103-16 - PubMed
  40. J Neurophysiol. 2012 Jun;107(11):3008-19 - PubMed
  41. Front Neural Circuits. 2013 Feb 07;7:13 - PubMed
  42. J Physiol. 1987 Apr;385:733-59 - PubMed
  43. J Neurosci. 2002 Dec 15;22(24):11019-25 - PubMed
  44. Eur J Neurosci. 2004 Sep;20(5):1318-30 - PubMed
  45. EMBO J. 2000 Jun 1;19(11):2483-91 - PubMed
  46. J Physiol. 2003 Apr 1;548(Pt 1):219-32 - PubMed
  47. J Neurosci. 2002 Aug 15;22(16):6953-61 - PubMed
  48. J Neurosci. 2005 Sep 21;25(38):8776-87 - PubMed
  49. J Physiol. 1971 Feb;213(1):31-53 - PubMed
  50. J Physiol. 2005 Nov 15;569(Pt 1):41-57 - PubMed
  51. J Comp Neurol. 1996 Mar 18;366(4):613-42 - PubMed
  52. J Neurosci. 2002 Feb 15;22(4):1256-65 - PubMed
  53. Nat Neurosci. 2010 Oct;13(10):1276-82 - PubMed
  54. J Neurosci. 2002 Dec 1;22(23):10106-15 - PubMed
  55. J Neurosci. 2003 Feb 15;23(4):1133-41 - PubMed
  56. Physiol Rev. 2010 Apr;90(2):559-605 - PubMed
  57. J Neurophysiol. 1999 Apr;81(4):1802-9 - PubMed
  58. Proc Natl Acad Sci U S A. 2006 Jan 24;103(4):1088-93 - PubMed

Publication Types

Grant support