Везде

RAS BiologyБиологические мембраны Membrane and Cell Biology

  • ISSN (Print) 0233-4755
  • ISSN (Online) 3034-5219

Comparison of spontaneous and evoked activity of CA1 pyramidal cells and dentate gyrus granule cells of the hippocampus at an increased extracellular potassium concentration

You can
PII
S0233475525010069-1
DOI
10.31857/S0233475525010069
Publication type
Article
Status
Published
Authors
A. S. Galashin
  • Affiliation: Institute of Theoretical and Experimental Biophysics, Russian Academy of Sciences
Volume/ Edition
Volume 42 / Issue number 1
Pages
61-70
Abstract
We studied the effect of changing extracellular potassium concentration ([K+]o) on spontaneous and evoked burst activity of glutamatergic neurons in the mouse hippocampus using whole-cell patch clamp. We show that increasing [K+]o from 3 to 8.5 mM (potassium load) induced spontaneous tonic (1) and pacemaker burst (2) activity of CA1 pyramidal cells (20% and 10% of the total number of cells, respectively). In contrast to CA1, potassium loading did not lead to the appearance of pacemaker granule cells in the dentate gyrus (DG). Similarly, potassium load increased the evoked burst activity of CA1 pyramidal cells and, paradoxically, suppressed the burst activity of DG granule cells over the entire range of current steps from 10 to 200 pA. Potassium load shifted the current-voltage characteristics to the right and substantially increased inward currents in CA1 and DG cells. Inward and outward currents of DG neurons were 4–4.5 times as high as those of CA1 cells. The possible involvement of potassium-activated potassium-conducting channels is discussed in the bimodal effect of potassium load on the excitability of CA1 and DG glutamatergic neurons. Our results suggest that CA1 pyramidal cells may be more sensitive to potassium load than DG granule cells, which may play a role in hyperexcitation of neural networks during epileptogenesis.
Keywords
пэтч-кламп пирамидные и гранулярные клетки поле СА1 и зубчатая извилина гиппокампа калиевая нагрузка пейсмейкерные пирамидные клетки
Date of publication
17.09.2025
Year of publication
2025
Number of purchasers
0
Views
17

References

  1. 1. Shao J., Liu Y., Gao D., Tu J., Yang F. 2021. Neural Burst Firing and Its Roles in Mental and Neurological Disorders. Front. Cell. Neurosci., 15, 741292. doi 10.3389/fncel.2021.741292
  2. 2. Targa Dias Anastacio H., Matosin N., Ooi L. 2022. Neuronal hyperexcitability in Alzheimer’s disease: what are the drivers behind this aberrant phenotype? Transl. Psychiatry, 12, 257. doi 10.1038/s41398-022-02024-7
  3. 3. Telias M., Segal M. 2022. Editorial: Pathological hyperactivity and hyperexcitability in the central nervous system. Front. Mol. Neurosci., 15, 955542. doi 10.3389/fnmol.2022.955542
  4. 4. Raimondo J.V., Burman R.J., Katz A.A., Akerman C.J. 2015. Ion dynamics during seizures. Front. Cell. Neurosci. 9, 419. doi 10.3389/fncel.2015.00419
  5. 5. Antonio L.L., Anderson M.L., Angamo E.A., Gabriel S., Klaft Z.-J., Liotta A., Salar S., Sandow N., Heinemann U. 2016. In vitro seizure like events and changes in ionic concentration. J. Neurosci. Methods. 260, 33–44. doi 10.1016/j.jneumeth.2015.08.014
  6. 6. Rasmussen R., O’Donnell J., Ding F., Nedergaard M. 2020. Interstitial ions: A key regulator of state-dependent neural activity? Prog. Neurobiol. 193, 101802. doi 10.1016/j.pneurobio.2020.101802
  7. 7. de Curtis M., Uva L., Gnatkovsky V., Librizzi L. 2018. Potassium dynamics and seizures: Why is potassium ictogenic? Epilepsy Res. 143, 50–59. doi 10.1016/j.eplepsyres.2018.04.005
  8. 8. Fertziger A.P., Ranck J.B. 1970. Potassium accumulation in interstitial space during epileptiform seizures. Exp. Neurol. 26, 571–585. doi 10.1016/0014-4886(70)90150-0
  9. 9. Zuckermann E.C., Glaser G.H. 1968. Hippocampal epileptic activity induced by localized ventricular perfusion with high-potassium cerebrospinal fluid. Exp. Neurol. 20, 87–110. doi 10.1016/0014-4886(68)90126-x
  10. 10. Traynelis S.F., Dingledine R. 1988. Potassium-induced spontaneous electrographic seizures in the rat hippocampal slice. J. Neurophysiol. 59, 259–276. doi 10.1152/jn.1988.59.1.259
  11. 11. Somjen G.G., Müller M. 2000. Potassium-induced enhancement of persistent inward current in hippocampal neurons in isolation and in tissue slices. Brain Res. 885, 102–110. doi 10.1016/s0006-8993(00)02948-6
  12. 12. Wang L., Dufour S., Valiante T.A., Carlen P.L. 2016. Extracellular Potassium and Seizures: Excitation, Inhibition and the Role of Ih. Int. J. Neural. Syst. 26, 1650044. doi 10.1142/S0129065716500441
  13. 13. Liotta A., Caliskan G., ul Haq R., Hollnagel J.O., Rösler A., Heinemann U., Behrens C.J. 2011. Partial disinhibition is required for transition of stimulus-induced sharp wave-ripple complexes into recurrent epileptiform discharges in rat hippocampal slices. J. Neurophysiol. 105, 172–187. doi 10.1152/jn.00186.2010
  14. 14. Hablitz J.J., Johnston D. 1981. Endogenous nature of spontaneous bursting in hippocampal pyramidal neurons. Cell. Mol. Neurobiol. 1, 325–334. doi 10.1007/BF00716267
  15. 15. Pan E., Stringer J.L. 1997. Role of potassium and calcium in the generation of cellular bursts in the dentate gyrus. J. Neurophysiol. 77, 2293–2299. doi 10.1152/jn.1997.77.5.2293
  16. 16. Jensen M.S., Yaari Y. 1997. Role of intrinsic burst firing, potassium accumulation, and electrical coupling in the elevated potassium model of hippocampal epilepsy. J. Neurophysiol. 77, 1224–1233. doi 10.1152/jn.1997.77.3.1224
  17. 17. Lee-Liu D., Gonzalez-Billault C. 2021. Neuron-intrinsic origin of hyperexcitability during early pathogenesis of Alzheimer’s disease: An Editorial Highlight for ‘Hippocampal hyperactivity in a rat model of Alzheimer’s disease’ on https://doi.org/10.1111/jnc.15323. J. Neurochem., 158, 586–588. doi 10.1111/jnc.15248
  18. 18. Sanabria E.R., Su H., Yaari Y. 2001. Initiation of network bursts by Ca2+-dependent intrinsic bursting in the rat pilocarpine model of temporal lobe epilepsy. J. Physiol., 532, 205–216. doi 10.1111/j.1469-7793.2001.0205g.x
  19. 19. Hofer K.T., Kandrács Á., Tóth K., Hajnal B., Bokodi V., Tóth E.Z., Erőss L., Entz L., Bagó A.G., Fabó D., Ulbert I., Wittner L. 2022. Bursting of excitatory cells is linked to interictal epileptic discharge generation in humans. Sci. Rep., 12, 6280. doi 10.1038/s41598-022-10319-4
  20. 20. David Y., Cacheaux L.P., Ivens S., Lapilover E., Heinemann U., Kaufer D., Friedman A. 2009. Astrocytic dysfunction in epileptogenesis: Consequence of altered potassium and glutamate homeostasis? J. Neurosci. 29, 10588–10599. doi 10.1523/JNEUROSCI.2323-09.2009
  21. 21. de Curtis M., Librizzi L., Uva L. 2006. In Vitro Isolated Guinea Pig Brain. In: Models of Seizures and Epilepsy. Academic Press Inc., p. 103–109.
  22. 22. Fröhlich F., Bazhenov M., Iragui-Madoz V., Sejnowski T.J. 2008. Potassium dynamics in the epileptic cortex: New insights on an old topic. Neuroscientist. 14, 422–433. doi 10.1177/1073858408317955
  23. 23. González O.C., Shiri Z., Krishnan G.P., Myers T.L., Williams S., Avoli M., Bazhenov M. 2018. Role of KCC2-dependent potassium efflux in 4-Aminopyridine-induced Epileptiform synchronization. Neurobiol. Dis. 109, 137–147. doi 10.1016/j.nbd.2017.10.011
  24. 24. Gentiletti D., de Curtis M., Gnatkovsky V., Suffczynski P. 2022. Focal seizures are organized by feedback between neural activity and ion concentration changes. Elife. 11, e68541. doi 10.7554/eLife.68541
  25. 25. Nenov M.N., Tempia F., Denner L., Dineley K.T., Laezza F. 2015. Impaired firing properties of dentate granule neurons in an Alzheimer's disease animal model are rescued by PPARγ agonism. J. Neurophysiol. 113 (6), 1712–26. doi 10.1152/jn.00419.2014
  26. 26. Tamagnini F., Scullion S., Brown J.T., Randall A.D. 2015. Intrinsic excitability changes induced by acute treatment of hippocampal CA1 pyramidal neurons with exogenous amyloid β peptide. Hippocampus. 25 (7), 786–97. doi 10.1002/hipo.22403
  27. 27. Harden S.W. pyABF: A pure-Python ABF file reader. URL: https://pypi.org/project/pyabf/ [date accessed: 05.05.2024]
  28. 28. Bikson M., Hahn P.J., Fox J.E., Jefferys J. 2003. Depolarization block of neurons during maintenance of electrographic seizures. J. Neurophysiol. 90 (4), 2402–8. doi 10.1152/jn.00467.2003
  29. 29. Averin A.S., Konakov M.V., Pimenov O.Y., Galimova M.H., Berezhnov A.V., Nenov M.N., Dynnik V.V. 2022. Regulation of papillary muscle contractility by NAD and ammonia interplay: Contribution of ion channels and exchangers. Membranes (Basel). 12 (12), 1239. doi 10.3390/membranes12121239
  30. 30. Yamashita T., Horio Y., Yamada M., Takahashi N., Kondo C., Kurachi Y. 1996. Competition between Mg2+ and spermine for a cloned IRK2 channel expressed in a human cell line. J. Physiol. 493 (Pt 1), 143–156. doi 10.1113/jphysiol.1996.sp021370
  31. 31. Ishihara K., Ehara T. 1998. A repolarization-induced transient increase in the outward current of the inward rectifier K+ channel in guinea-pig cardiac myocytes. J. Physiol. 510 (Pt 3), 755–771. doi 10.1111/j.1469-7793.1998.755bj.x
  32. 32. Dhamoon A.S., Pandit S.V., Sarmast F., Parisian K.R., Guha P., Li Y., Bagwe S., Taffet S.M., Anumonwo J.M.B. 2004. Unique Kir2.x properties determine regional and species differences in the cardiac inward rectifier K+ current. Circ. Res. 94, 1332–1339. doi 10.1161/01.RES.0000128408.66946.67
  33. 33. McCormick D.A., Pape H.C. 1990. Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic relay neurones. J. Physiol. 431, 291–318. doi 10.1113/jphysiol.1990.sp018331
  34. 34. Azene E.M., Xue T., Li R.A. 2003. Molecular basis of the effect of potassium on heterologously expressed pacemaker (HCN) channels. J. Physiol. 547, 349–356. doi 10.1113/jphysiol.2003.039768
  35. 35. Nuss H.B., Marbán E., Johns D.C. 1999. Overexpression of a human potassium channel suppresses cardiac hyperexcitability in rabbit ventricular myocytes. J. Clin. Invest. 103, 889–896. doi 10.1172/JCI5073
  36. 36. Arima-Yoshida F., Watabe A.M., Manabe T. 2011. The mechanisms of the strong inhibitory modulation of long-term potentiation in the rat dentate gyrus. Eur. J. Neurosci. 33 (9), 1637–1646. doi 10.1111/j.1460-9568.2011.07657.x
  37. 37. Bertrand S., Nouel D., Morin F., Nagy F., Lacaille J.-C. 2003. Gabapentin actions on Kir3 currents and N-type Ca2+ channels via GABAB receptors in hippocampal pyramidal cells. Synapse. 50 (2), 95–109. doi 10.1002/syn.10247
  38. 38. Yarishkin O., Lee D.Y., Kim E., Cho C.-H., Choi J.H., Lee C.J., Hwang E.M., Park J.-Y. 2014. TWIK-1 contributes to the intrinsic excitability of dentate granule cells in mouse hippocampus. Mol. Brain. 7, 80. doi 10.1186/s13041-014-0080-z
  39. 39. Bauer C.K., Schwarz J.R. 2018. Ether-à-Go-Go K+ channels: Effective modulators of neuronal excitability. J. Physiol. 596 (5), 769–783. doi 10.1113/JP275477
  40. 40. Mishra P., Narayanan R. 2021. Ion-channel degeneracy: Multiple ion channels heterogeneously regulate intrinsic physiology of rat hippocampal granule cells. Physiol. Rep. 9, e14963. doi 10.14814/phy2.14963
  41. 41. Bianchi D., Marasco A., Limongiello A., Marchetti C., Marie H., Tirozzi B., Migliore M. 2012. On the mechanisms underlying the depolarization block in the spiking dynamics of CA1 pyramidal neurons. J. Comput. Neurosci. 33 (2), 207–25. doi 10.1007/s10827-012-0383-y
  42. 42. Goaillard J.-M., Marder E. 2021. Ion channel degeneracy, variability, and covariation in neuron and circuit resilience. Annu. Rev. Neurosci. 44, 335–357. doi 10.1146/annurev-neuro-092920-121538
QR
Translate

Индексирование

Scopus

Scopus

Scopus

Crossref

Scopus

Higher Attestation Commission

At the Ministry of Education and Science of the Russian Federation

Scopus

Scientific Electronic Library