Diversity of Dynamic Voltage Patterns in Neuronal Dendrites Revealed by Nanopipette Electrophysiology

Overview

Journal Nanoscale

Specialty Biotechnology

Date 2023 Jul 17

PMID 37455621

Authors

Jeffrey Mc Hugh

Stanislaw Makarchuk

Daria Mozheiko

Ana Fernandez-Villegas

Gabriele S Kaminski Schierle

Clemens F Kaminski

Ulrich F Keyser

David Holcman

Nathalie Rouach

Affiliations

Soon will be listed here.

Abstract

Dendrites and dendritic spines are the essential cellular compartments in neuronal communication, conveying information through transient voltage signals. Our understanding of these compartmentalized voltage dynamics in fine, distal neuronal dendrites remains poor due to the difficulties inherent to accessing and stably recording from such small, nanoscale cellular compartments for a sustained time. To overcome these challenges, we use nanopipettes that permit long and stable recordings directly from fine neuronal dendrites. We reveal a diversity of voltage dynamics present locally in dendrites, such as spontaneous voltage transients, bursting events and oscillating periods of silence and firing activity, all of which we characterized using segmentation analysis. Remarkably, we find that neuronal dendrites can display spontaneous hyperpolarisation events, and sustain transient hyperpolarised states. The voltage patterns were activity-dependent, with a stronger dependency on synaptic activity than on action potentials. Long-time recordings of fine dendritic protrusions show complex voltage dynamics that may represent a previously unexplored contribution to dendritic computations.

References

Neher E, Sakmann B . Single-channel currents recorded from membrane of denervated frog muscle fibres. Nature. 1976; 260(5554):799-802. DOI: 10.1038/260799a0. View

Jayant K, Wenzel M, Bando Y, Hamm J, Mandriota N, Rabinowitz J . Flexible Nanopipettes for Minimally Invasive Intracellular Electrophysiology In Vivo. Cell Rep. 2019; 26(1):266-278.e5. PMC: 7263204. DOI: 10.1016/j.celrep.2018.12.019. View

Cornejo V, Ofer N, Yuste R . Voltage compartmentalization in dendritic spines in vivo. Science. 2021; 375(6576):82-86. PMC: 8942082. DOI: 10.1126/science.abg0501. View

Marbach S . Intrinsic fractional noise in nanopores: The effect of reservoirs. J Chem Phys. 2021; 154(17):171101. DOI: 10.1063/5.0047380. View

London M, Hausser M . Dendritic computation. Annu Rev Neurosci. 2005; 28:503-32. DOI: 10.1146/annurev.neuro.28.061604.135703. View

Novak P, Gorelik J, Vivekananda U, Shevchuk A, Ermolyuk Y, Bailey R . Nanoscale-targeted patch-clamp recordings of functional presynaptic ion channels. Neuron. 2013; 79(6):1067-77. PMC: 3781326. DOI: 10.1016/j.neuron.2013.07.012. View

Knowles S, Weckman N, Lim V, Bonthuis D, Keyser U, Thorneywork A . Current Fluctuations in Nanopores Reveal the Polymer-Wall Adsorption Potential. Phys Rev Lett. 2021; 127(13):137801. DOI: 10.1103/PhysRevLett.127.137801. View

Jayant K, Hirtz J, Jen-La Plante I, Tsai D, de Boer W, Semonche A . Targeted intracellular voltage recordings from dendritic spines using quantum-dot-coated nanopipettes. Nat Nanotechnol. 2016; 12(4):335-342. PMC: 5901699. DOI: 10.1038/nnano.2016.268. View

Perez-Reyes E . Molecular physiology of low-voltage-activated t-type calcium channels. Physiol Rev. 2002; 83(1):117-61. DOI: 10.1152/physrev.00018.2002. View

10.

Beaulieu-Laroche L, Toloza E, van der Goes M, Lafourcade M, Barnagian D, Williams Z . Enhanced Dendritic Compartmentalization in Human Cortical Neurons. Cell. 2018; 175(3):643-651.e14. PMC: 6197488. DOI: 10.1016/j.cell.2018.08.045. View

11.

Dan O, Hopp E, Borst A, Segev I . Non-uniform weighting of local motion inputs underlies dendritic computation in the fly visual system. Sci Rep. 2018; 8(1):5787. PMC: 5893613. DOI: 10.1038/s41598-018-23998-9. View

12.

Angle M, Cui B, Melosh N . Nanotechnology and neurophysiology. Curr Opin Neurobiol. 2015; 32:132-40. DOI: 10.1016/j.conb.2015.03.014. View

13.

Chua J, Kindler S, Boyken J, Jahn R . The architecture of an excitatory synapse. J Cell Sci. 2010; 123(Pt 6):819-23. DOI: 10.1242/jcs.052696. View

14.

Sohl G, Maxeiner S, Willecke K . Expression and functions of neuronal gap junctions. Nat Rev Neurosci. 2005; 6(3):191-200. DOI: 10.1038/nrn1627. View

15.

Magistretti J, Mantegazza M, Guatteo E, Wanke E . Action potentials recorded with patch-clamp amplifiers: are they genuine?. Trends Neurosci. 1996; 19(12):530-4. DOI: 10.1016/s0166-2236(96)40004-2. View

16.

Ujfalussy B, Makara J, Lengyel M, Branco T . Global and Multiplexed Dendritic Computations under In Vivo-like Conditions. Neuron. 2018; 100(3):579-592.e5. PMC: 6226578. DOI: 10.1016/j.neuron.2018.08.032. View

17.

Kandel E, Spencer W . Electrophysiology of hippocampal neurons. II. After-potentials and repetitive firing. J Neurophysiol. 1961; 24:243-59. DOI: 10.1152/jn.1961.24.3.243. View

18.

COOMBS J, ECCLES J, FATT P . The specific ionic conductances and the ionic movements across the motoneuronal membrane that produce the inhibitory post-synaptic potential. J Physiol. 1955; 130(2):326-74. PMC: 1363415. DOI: 10.1113/jphysiol.1955.sp005412. View

19.

Dossi E, Blauwblomme T, Moulard J, Chever O, Vasile F, Guinard E . Pannexin-1 channels contribute to seizure generation in human epileptic brain tissue and in a mouse model of epilepsy. Sci Transl Med. 2018; 10(443). DOI: 10.1126/scitranslmed.aar3796. View

20.

Eyal G, Mansvelder H, de Kock C, Segev I . Dendrites impact the encoding capabilities of the axon. J Neurosci. 2014; 34(24):8063-71. PMC: 6608238. DOI: 10.1523/JNEUROSCI.5431-13.2014. View