Abstract
Birds have ten pairs of protrusions, “accessory lobes”, on the lateral sides of the lumbosacral spinal cord. It has been proposed that accessory lobes act as a sensory organ of equilibrium and neurons in accessory lobes transmit sensory information to the motor center. We have reported that cells in chick accessory lobes express functional voltage-gated Na+ and K+ channels and generate action potentials. In this study, we examined properties of voltage-gated Ca2+ channels (VGCCs). The amplitude of voltage-gated Ca2+ channel currents carried by Ca2+ and Ba2+ increased gradually during 10 min rather than showing the usual run-down. The current–voltage relationship of Ba2+ currents was consistent with that of the high-voltage-activated Ca2+ channel. The proportion of Ba2+ currents inhibited by ω-conotoxin GVIA was larger than 80 %, indicating that the major subtype is N type. Amplitudes of tail currents of Ca2+ currents evoked by repetitive pulses at 50 Hz are stable for 1 s. If the major subtype of VGCCs at synaptic terminals is also N type, this property may contribute to the establishment of stable synaptic connections between accessory lobe neurons, which are reported to fire at frequencies higher than 15 Hz, and postsynaptic neurons in the spinal cord.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- AL:
-
Accessory lobe
- AP:
-
Action potential
- I Ba :
-
Ba2+ current
- I Ca :
-
Ca2+ current
- I VGCC :
-
Voltage-gated Ca2+ channel current
- VGCC:
-
Voltage-gated Ca2+ channel
References
Aosaki T, Kasai H (1989) Characterization of two kinds of high-voltage-activated Ca-channel currents in chick sensory neurons. Differential sensitivity to dihydropyridines and ω-conotoxin GVIA. Pflügers Arch 414:150–156
Benton MD, Raman IM (2009) Stabilization of Ca current in Purkinje neurons during high-frequency firing by a balance of Ca-dependent facilitation and inactivation. Channels 3:393–401
Bolsover SR, Spector I (1986) Measurements of calcium transients in the soma, neurite, and growth cone of single cultured neurons. J Neurosci 6:1934–1940
Carbone E, Lux HD (1984) A low voltage-activated calcium conductance in embryonic chick sensory neurons. Biophys J 46:413–418
Catterall WA (1999) Interactions of presynaptic Ca2+ channels and snare proteins in neurotransmitter release. Ann N Y Acad Sci 868:144–159
Catterall WA, Perez-Reyes E, Snutch TP, Striessnig J (2005) International union of pharmacology. XLVIII. Nomenclature and structure–function relationships of voltage-gated calcium channels. Pharmacol Rev 57:411–425
Cens T, Rousset M, Leyris JP, Fesquet P, Charnet P (2006) Voltage- and calcium-dependent inactivation in high voltage-gated Ca2+ channels. Prog Biophys Mol Biol 90:104–117
Christel C, Lee A (2012) Ca2+-dependent modulation of voltage-gated Ca2+ channels. Biochim Biophys Acta 1820:1243–1252
Cox DH, Dunlap K (1992) Pharmacological discrimination of N-type from L-type calcium current and its selective modulation by transmitters. J Neurosci 12:906–914
Currie KP (2010) G protein modulation of CaV2 voltage-gated calcium channels. Channels 4:497–509
Dove LS, Abbott LC, Griffith WH (1998) Whole-cell and single-channel analysis of P-type calcium currents in cerebellar Purkinje cells of leaner mutant mice. J Neurosci 18:7687–7699
Dunlap K, Luebke JI, Turner TJ (1995) Exocytotic Ca2+ channels in mammalian central neurons. Trends Neurosci 18:89–98
Gamper N, Reznikov V, Yamada Y, Yang J, Shapiro MS (2004) Phosphatidylinositol 4,5-bisphosphate signals underlie receptor-specific Gq/11-mediated modulation of N-type Ca2+ channels. J Neurosci 24:10980–10992
Ikeda SR (1996) Voltage-dependent modulation of N-type calcium channels by G-protein βγ subunits. Nature 380:255–258
Ikeda SR, Dunlap K (1999) Voltage-dependent modulation of N-type calcium channels: role of G protein subunits. Adv Second Messenger Phosphoprotein Res 33:131–151
Kitamura N, Ohta T, Ito S, Nakazato Y (1998) Calcium channel current facilitation in porcine adrenal chromaffin cells. Pflügers Arch 435:781–788
Lachi P (1889) Alcune particolarita anatomiche del rigonfiamento sacrale nel midollo degli uccelli. Lobi accessori. Att Soc Tosc Sci Nat 10:268–295
McCobb DP, Beam KG (1991) Action potential waveform voltage-clamp commands reveal striking differences in calcium entry via low and high voltage-activated calcium channels. Neuron 7:119–127
Necker R (1999) Specializations in the lumbosacral spinal cord of birds: morphological and behavioural evidence for a sense of equilibrium. Eur J Morphol 37:211–214
Necker R (2004) Histological and immunocytochemical characterization of neurons located in the white matter of the spinal cord of the pigeon. J Chem Neuroanat 27:109–117
Necker R (2005) The structure and development of avian lumbosacral specializations of the vertebral canal and the spinal cord with special reference to a possible function as a sense organ of equilibrium. Anat Embryol (Berl) 210:59–74
Necker R (2006) Specializations in the lumbosacral vertebral canal and spinal cord of birds: evidence of a function as a sense organ which is involved in the control of walking. J Comp Physiol A 192:439–448
Necker R, Janßen A, Beissenhirtz T (2000) Behavioral evidence of the role of lumbosacral anatomical specializations in pigeons in maintaining balance during terrestrial locomotion. J Comp Physiol A 186:409–412
Pietrobon D (2005) Function and dysfunction of synaptic calcium channels: insights from mouse models. Curr Opin Neurobiol 15:257–265
Rabbitt RD, Highstein SM, Boyle R (1996) Determinants of semicircular canal afferent response dynamics in fish. Ann N Y Acad Sci 781:213–243
Rabbitt RD, Boyle R, Holstein GR, Highstein SM (2005) Hair-cell versus afferent adaptation in the semicircular canals. J Neurophysiol 93:424–436
Rodriguez-Menchaca AA, Adney SK, Zhou L, Logothetis DE (2012) Dual regulation of voltage-sensitive ion channels by PIP2. Front Pharmacol 3:170
Rosenberg J, Necker R (2000) Fine structural evidence of mechanoreception in spinal lumbosacral accessory lobes of pigeons. Neurosci Lett 285:13–16
Rosenberg J, Necker R (2002) Ultrastructural characterization of the accessory lobes of Lachi in the lumbosacral spinal cord of the pigeon with special reference to intrinsic mechanoreceptors. J Comp Neurol 447:274–285
Wu L, Bauer CS, Zhen XG, Xie C, Yang J (2002) Dual regulation of voltage-gated calcium channels by PtdIns(4,5)P2. Nature 419:947–952
Yamanaka Y, Kitamura N, Shibuya I (2008) Chick spinal accessory lobes contain functional neurons expressing voltage-gated sodium channels generating action potentials. Biomed Res 29:205–211
Yamanaka Y, Kitamura N, Shinohara H, Takahashi K, Shibuya I (2012) Analysis of GABA-induced inhibition of spontaneous firing in chick accessory lobe neurons. J Comp Physiol A 198:229–237
Yamanaka Y, Kitamura N, Shinohara H, Takahashi K, Shibuya I (2013) Glutamate evokes firing through activation of kainate receptors in chick accessory lobe neurons. J Comp Physiol A 199:35–43
Zhen XG, Xie C, Yamada Y, Zhang Y, Doyle C, Yang J (2006) A single amino acid mutation attenuates rundown of voltage-gated calcium channels. FEBS Lett 580:5733–5738
Acknowledgments
We are grateful to Dr. Sam Kongsamut for critical reading of the manuscript. The animal experiments were performed in accordance with the guidelines stipulated by the ethical committee of Tottori University. This work is supported by KAKENHI provided by Japan Society for the Promotion of Science; Grant No: 25450463, 25450464.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Suzuki, Y., Kitamura, N., Yamanaka, Y. et al. Voltage-gated Ca2+ channels in accessory lobe neurons of the chick. J Comp Physiol A 200, 739–748 (2014). https://doi.org/10.1007/s00359-014-0917-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-014-0917-z