Afterhyperpolarization (AHP) regulates the frequency and timing of action potentials in the mitral cells of the olfactory bulb: Role of olfactory experience

Physiological Reports

Volumn 3, Issue 5, 2015, Pages

  Duménieu, Maël ^a   Fourcaud Trocmé, Nicolas ^a   Garcia, Samuel ^a   Kuczewski, Nicola ^a  

^a UNIVERSITÉ LYON 1   (France)

Author keywords

Firing; Intrinsic plasticity; Recurrent synaptic transmission

Indexed keywords

ACTION POTENTIAL DURATION; AFTERHYPERPOLARIZATION; AGE; ANIMAL EXPERIMENT; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CALCIUM TRANSPORT; CONTROLLED STUDY; EPIFLUORESCENCE MICROSCOPY; GABAERGIC SYSTEM; GLUTAMATERGIC SYNAPSE; HYPERPOLARIZATION; IMAGE RECONSTRUCTION; LATENT PERIOD; MALE; MITRAL CELL; NEUROMODULATION; NONHUMAN; ODOR; OLFACTORY BULB; RAT; SMELLING; SYNAPTIC TRANSMISSION;

EID: 84947462695     PISSN: None     EISSN: 2051817X     Source Type: Journal    
DOI: 10.14814/phy2.12344     Document Type: Article

References (56)

1. Angelo, K., and T. W. Margrie. 2011. Population diversity and function of hyperpolarization-activated current in olfactory bulb mitral cells. Sci. Rep. 1:50.
2. Apicella, A., Q. Yuan, M. Scanziani, and J. S. Isaacson. 2010. Pyramidal cells in piriform cortex receive convergent input from distinct olfactory bulb glomeruli. J. Neurosci. 30:14255–14260.
3. Arevian, A. C., V. Kapoor, and N. N. Urban. 2008. Activitydependent gating of lateral inhibition in the mouse olfactory bulb. Nat. Neurosci. 11:80–87.
4. Aroniadou-Anderjaska, V., M. Ennis, and M. T. Shipley. 1999. Dendrodendritic recurrent excitation in mitral cells of the rat olfactory bulb. J. Neurophysiol. 82:489–494.
5. Balu, R., P. Larimer, and B. W. Strowbridge. 2004. Phasic stimuli evoke precisely timed spikes in intermittently discharging mitral cells. J. Neurophysiol. 92:743–753.
6. Balu, R., R. T. Pressler, and B. W. Strowbridge. 2007. Multiple modes of synaptic excitation of olfactory bulb granule cells. J. Neurosci. 27:5621–5632.
7. Bathellier, B., O. Gschwend and A. Carleton. 2010. Temporal coding in olfaction. Pp. 329–352 in A. Menini, ed. The neurobiology of olfaction, frontiers in neuroscience. CRC Press, Boca Raton, FL.
8. Behr, J., T. Gloveli, and U. Heinemann. 2000. Kindling induces a transient suppression of after hyperpolarization in rat subicular neurons. Brain Res. 867:259–264.
9. Ben-Ari, Y., J.-L. Gaiarsa, R. Tyzio, and R. Khazipov. 2007. GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol. Rev. 87:1215–1284.
10. Berridge, M. J. 2006. Calcium microdomains: organization and function. Cell Calcium 40:405–412.
11. Boyd, A. M., J. F. Sturgill, C. Poo, and J. S. Isaacson. 2012. Cortical feedback control of olfactory bulb circuits. Neuron 76:1161–1174.
12. Briffaud, V., N. Fourcaud-Trocmé, B. Messaoudi, N. Buonviso, and C. Amat. 2012. The relationship between respirationrelated membrane potential slow oscillations and discharge patterns in mitral/tufted cells: what are the rules? PLoS ONE 7:e43964.
13. Buonviso, N., and M. Chaput. 2000. Olfactory experience decreases responsiveness of the olfactory bulb in the adult rat. Neuroscience 95:325–332.
14. Buonviso, N., R. Gervais, M. Chalansonnet, and M. Chaput. 1998. Short-lasting exposure to one odour decreases general reactivity in the olfactory bulb of adult rats. Eur. J. Neurosci. 10:2472–2475.
15. Castro, J. B., K. R. Hovis, and N. N. Urban. 2007. Recurrent dendrodendritic inhibition of accessory olfactory bulb mitral cells requires activation of group I metabotropic glutamate receptors. J. Neurosci. 27:5664–5671.
16. Courtiol, E., C. Hegoburu, P. Litaudon, S. Garcia, N. Fourcaud-Trocmé, and N. Buonviso. 2011. Individual and synergistic effects of sniffing frequency and flow rate on olfactory bulb activity. J. Neurophysiol. 106:2813–2824.
17. David, F., C. Linster, and T. A. Cleland. 2008. Lateral dendritic shunt inhibition can regularize mitral cell spike patterning. J. Comput. Neurosci. 25:25–38.
18. Dietz, S. B., F. Markopoulos, and V. N. Murthy. 2011. Postnatal development of dendrodendritic inhibition in the Mammalian olfactory bulb. Front. Cell. Neurosci. 5:10.
19. Doucette, W., D. H. Gire, J. Whitesell, V. Carmean, M. T. Lucero, and D. Restrepo. 2011. Associative cortex features in the first olfactory brain relay station. Neuron 69:1176–1187.
20. Faber, E. S., and P. Sah. 2007. Functions of SK channels in central neurons. Clin. Exp. Pharmacol. Physiol. 34:1077–1083.
21. Fadool, D. A., K. Tucker, and P. Pedarzani. 2011. Mitral cells of the olfactory bulb perform metabolic sensing and are disrupted by obesity at the level of the Kv1.3 ion channel. PLoS ONE 6:e24921.
22. Friedman, D., and B. W. Strowbridge. 2000. Functional role of NMDA autoreceptors in olfactory mitral cells. J. Neurophysiol. 84:39–50.
23. Fukunaga, I., M. Berning, M. Kollo, A. Schmaltz, and A. T. Schaefer. 2012. Two distinct channels of olfactory bulb output. Neuron. 75:320–329.
24. Garcia, S., and N. Fourcaud-Trocmé. 2009. OpenElectrophy: an electrophysiological data- and analysis-sharing framework. Front. Neuroinform. 3:14.
25. Gasparini, S., and D. DiFrancesco. 1999. Action of serotonin on the hyperpolarization-activated cation current (Ih) in rat CA1 hippocampal neurons. Eur. J. Neurosci. 11:3093–3100.
26. Gerkin, R. C., S. J. Tripathy, and N. N. Urban. 2013. Origins of correlated spiking in the mammalian olfactory bulb. Proc. Natl Acad. Sci. USA 110:17083–17088.
27. Ghatpande, A. S., K. Sivaraaman, and S. Vijayaraghavan. 2006. Store calcium mediates cholinergic effects on mIPSCs in the rat main olfactory bulb. J. Neurophysiol. 95:1345–1355.
28. Gschwend, O., J. Beroud, and A. Carleton. 2012. Encoding odorant identity by spiking packets of rate-invariant neurons in awake mice. PLoS ONE 7:e30155.
29. Halabisky, B., and B. W. Strowbridge. 2003. Gamma-frequency excitatory input to granule cells facilitates dendrodendritic inhibition in the rat olfactory Bulb. J. Neurophysiol. 90:644–654.
30. Isaacson, J. S., and B. W. Strowbridge. 1998. Olfactory reciprocal synapses: dendritic signaling in the CNS. Neuron 20:749–761.
31. Jahr, C. E., and R. A. Nicoll. 1982. Noradrenergic modulation of dendrodendritic inhibition in the olfactory bulb. Nature 297:227–229.
32. Kay, L. M., J. Beshel, J. Brea, C. Martin, D. Rojas-Líbano, and N. Kopell. 2009. Olfactory oscillations: the what, how and what for. Trends Neurosci. 32:207–214.
33. Laurent, G. 2002. Olfactory network dynamics and the coding of multidimensional signals. Nat. Rev. Neurosci. 3:884–895.
34. Maccaferri, G., and C. J. McBain. 1996. The hyperpolarizationactivated current (Ih) and its contribution to pacemaker activity in rat CA1 hippocampal stratum oriens-alveus interneurones. J. Physiol. 497(Pt 1):119–130.
35. Maher, B. J., and G. L. Westbrook. 2005. SK channel regulation of dendritic excitability and dendrodendritic inhibition in the olfactory bulb. J. Neurophysiol. 94:3743–3750.
36. Malun, D., and P. C. Brunjes. 1996. Development of olfactory glomeruli: temporal and spatial interactions between olfactory receptor axons and mitral cells in opossums and rats. J. Comp. Neurol. 368:1–16.
37. Margrie, T. W., and A. T. Schaefer. 2003. Theta oscillation coupled spike latencies yield computational vigour in a mammalian sensory system. J. Physiol. 546:363–374.
38. Moyer, J. R., L. T. Thompson, J. P. Black, and J. F. Disterhoft. 1992. Nimodipine increases excitability of rabbit CA1 pyramidal neurons in an age- and concentration-dependent manner. J. Neurophysiol. 68:2100–2109.
39. Neher, E., and G. J. Augustine. 1992. Calcium gradients and buffers in bovine chromaffin cells. J. Physiol. 450: 273–301.
40. Nolan, M. F., J. T. Dudman, P. D. Dodson, and B. Santoro. 2007. HCN1 channels control resting and active integrative properties of stellate cells from layer II of the entorhinal cortex. J. Neurosci. 27:12440–12451.
41. Otsuka, T., K. Ishii, Y. Osako, F. Okutani, M. Taniguchi, T. Oka, et al. 2001. Modulation of dendrodendritic interactions and mitral cell excitability in the mouse accessory olfactory bulb by vaginocervical stimulation. Eur. J. Neurosci. 13:1833–1838.
42. Padmanabhan, K., and N. N. Urban. 2010. Intrinsic biophysical diversity decorrelates neuronal firing while increasing information content. Nat. Neurosci. 13:1276–1282.
43. Ravel, N., P. Chabaud, C. Martin, V. Gaveau, E. Hugues, C. Tallon-Baudry, et al. 2003. Olfactory learning modifies the expression of odour-induced oscillatory responses in the gamma (60–90 Hz) and beta (15–40 Hz) bands in the rat olfactory bulb. Eur. J. Neurosci. 17:350–358.
44. Saar, D., and E. Barkai. 2009. Long-lasting maintenance of learning-induced enhanced neuronal excitability: mechanisms and functional significance. Mol. Neurobiol. 39:171–177.
45. Saar, D., Y. Grossman, and E. Barkai. 1998. Reduced after-hyperpolarization in rat piriform cortex pyramidal neurons is associated with increased learning capability during operant conditioning. Eur. J. Neurosci. 10: 1518–1523.
46. Sah, P. 1996. Ca(2+)-activated K+ currents in neurones: types, physiological roles and modulation. Trends Neurosci. 19:150–154.
47. Sah, P., and E. S. Faber. 2002. Channels underlying neuronal calcium-activated potassium currents. Prog. Neurobiol. 66:345–353.
48. Salin, P. A., P. M. Lledo, J. D. Vincent, and S. Charpak. 2001. Dendritic glutamate autoreceptors modulate signal processing in rat mitral cells. J. Neurophysiol. 85:1275–1282.
49. Schmid, S., and E. Guenther. 1996. Developmental regulation of voltage-activated Na+ and Ca2+ currents in rat retinal ganglion cells. NeuroReport 7:677–681.
50. Schoppa, N. E., J. M. Kinzie, Y. Sahara, T. P. Segerson, and G. L. Westbrook. 1998. Dendrodendritic inhibition in the olfactory bulb is driven by NMDA receptors. J. Neurosci. 18:6790–6802.
51. Shusterman, R., M. C. Smear, A. A. Koulakov, and D. Rinberg. 2011. Precise olfactory responses tile the sniff cycle. Nat. Neurosci. 14:1039–1044.
52. Stocker, M., M. Krause, and P. Pedarzani. 1999. An apaminsensitive Ca2+-activated K+ current in hippocampal pyramidal neurons. Proc. Natl Acad. Sci. USA 96:4662–4667.
53. Strowbridge, B. W. 2009. Role of cortical feedback in regulating inhibitory microcircuits. Ann. N. Y. Acad. Sci. 1170:270–274.
54. Uchida, N., C. Poo, and R. Haddad. 2014. Coding and transformations in the olfactory system. Annu. Rev. Neurosci. 37:363–385.
55. Wang, X. Y., J. S. McKenzie, and R. E. Kemm. 1996. Wholecell K+ currents in identified olfactory bulb output neurones of rats. J. Physiol. 490(Pt 1):63–77.
56. Zhan, C., and M. Luo. 2010. Diverse patterns of odor representation by neurons in the anterior piriform cortex of awake mice. J. Neurosci. 30:16662–16672.