Testing of the connections of Schaffer collaterals with field CA1 neurons in living slices of rat hippocampus was used to study the mechanism of deprivation potentiation (DeP) of population spikes developing as a result of a 60-min pause in stimulation (deprivation). Previous studies have shown that DeP has the property of input specificity and the ability to persist for prolonged periods; it consists of two components with independent mechanisms of induction: an initial short-term “peak” of presynaptic origin and a long-lasting “plateau” with a Ca2+-dependent postsynaptic mechanism mediated by P2 purine receptors. Studies of the properties of the input specificity of DeP were run using stimulation of two different populations of Schaffer collaterals and recording of pop-spikes in the general population of neurons in field CA1. These experiments showed that changes in synaptic efficiency in the deprived input depend only on a presynaptic mechanism responsible for the development of the short-term component of DeP. Studies of the postsynaptic mechanism of induction of the long-term component of DeP demonstrated that the function of the adenosine triphosphate (ATP) source required for activation of P2 purine receptors is mediated by pannexin-1, which forms ATP-conducting channels on the postsynapse. A working model of the cyclic mechanism of induction of the long-term component of DeP is presented.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
Tax calculation will be finalised during checkout.
Albers, R. W. and Siegel, G. J., “Membrane transport,” in: Basic Neurochemistry (molecular, cellular and medical aspects), G. J. Siegel (ed.), Elsevier Academic Press, New York (2006), pp. 73–94.
Attwell, D. and Laughlin, S. B., “An energy budget for signaling in the grey matter of the brain,” J. Cereb. Blood Flow Metab., 21, 1133–1145 (2001).
Bliss, T. V. P. and Lømo, T., “Long-lasting potentiation of synaptic transmission in the dentate area of the anesthetized rabbit following stimulation of the perforant path,” J. Physiol., 232, 331–356 (1973).
Boassa, D., Nguyen, Ph., Hu, J., et al., “Pannexin2 oligomers localize in the membranes of endosomal vesicles in mammalian cells while Pannexin1 channels traffic to the plasma membrane,” Front. Cell. Neurosci., 8, No. 468, 1–15 (2015).
Bond, S. R. and Naus, C. C., “The pannexins: past and present,” Front. Physiol., 5, No. 58, 1–24 (2014).
Burnstock, G. and Verkhratsky, A., Purinergic Signalling and the Nervous System, Springer-Verlag, Berlin (2012).
Burnstock, G., “Purinergic signalling: pathophysiology and therapeutic potential,” Keio J. Med., 62, No. 3, 63–73 (2013).
Dahl, G., “ATP release through pannexon channels,” Philos. Trans. R. Soc. Lond. B Biol. Sci., 370, No. 1672, 20140191 (2015).
Frey, U., Schollmeier, K., Reymann, K. G., and Seidenbecher, T., “Asymptotic hippocampal long-term potentiation in rats does not preclude additional potentiation at later phases,” Neuroscience, 67, No. 4, 799–807 (1995).
Li, S., Bjelobaba, I. and Stojilkovic, S. S., “Interactions of pannexin1 channels with purinergic and NMDA receptor channels,” Biochem. Biophys. Acta Biomembr., 1860, No. 1, 166–173 (2018).
Locovei, S., Wang, J., and Dahl, G., “Activation of pannexin 1 channels by ATP through P2Y receptors and by cytoplasmic calcium,” FEBS Lett., 580, No. 1, 239–244 (2006).
Lohman, A. W. and Isakson, B. E., “Differentiating connexin hemichannels and pannexin channels in cellular ATP release,” FEBS Lett., 588, 1379–1388 (2014).
Lohman, A. W., Weilingerc, N. L., Santos, S. M. F., et al., “Regulation of pannexin channels in the central nervous system by Src family kinases,” Neurosci. Lett., 695, 65–70 (2019).
Lynch, G. S., Dunwiddie, T., and Gribkoff, V., “Heterosynaptic depression: a postsynaptic correlate of long-term potentiation,” Nature, 266, 737–739 (1977).
Ma, W., Hui, H., Pelegrin, P., and Surprenant, A., “Pharmacological characterization of Pannexin-1 currents expressed in mammalian cells,” J. Pharmacol. Exp. Ther., 328, No. 2, 409–418 (2009).
McKenna, M. C., Dienel, G. A., Sonnewald, U., et al., “Energy metabolism of the brain,” in: Brady, S. T. et al. (eds), Basic Neurochemistry: Principles of Molecular, Cellular and Medical Neurobiology, Elsevier-Academic Press Amsterdam, Boston, Heidelberg, London, New York, Oxford, Paris, San Diego, San Francisco, Singapore, Sydney, Tokyo (2012), 8th ed., pp. 200–231.
Nelson, D. L. and Cox, M. M., Lehninger Principles of Biochemistry, W. H. Freeman and Company, New York (2013), 6th ed.
Panchin, Y., Kelmanson, I., Matz, M., et al., “Aubiquitous family of putative gap junction molecules,” Curr. Biol., 10, R473–R474 (2000).
Pankratov, Y., Lalo, U., Krishtal, O. A., and Verkhratsky, A., “P2X receptors and synaptic plasticity,” Neuroscientist, 158, No. 1, 137–148 (2009).
Parekh, A. B., “Decoding cytosolic Ca2+ oscillations,” Trends Biochem. Sci., 36, No. 2, 78–87 (2011).
Popov, V. A. and Markevich, V. A., “Development of slow potentiation of the population spike of the prolonged non-stimulated input in rats in the stage of anesthetic sleep,” Zh. Vyssh. Nerv. Deyat., 49, No. 4, 689–693 (1999).
Popov, V. A. and Markevich, V. A., “Studies of the mechanism of development of ‘deprivational’ potentiation of the population responses of neurons in field CA1 in living hippocampal slices,” Zh. Vyssh. Nerv. Deyat., 51, No. 5, 598–603 (2001).
Popov, V. A. and Markevich, V. A., “The key role of calcium in the mechanism of deprivational potentiation of the population responses of neurons in hippocampal field CA1,” Zh. Vyssh. Nerv. Deyat., 64, No. 1, 54–63 (2014).
Popov, V. A., “Pre- and postsynaptic mechanisms of deprivational potentiation of the population responses of neurons in rat hf CA1,” Zh. Vyssh. Nerv. Deyat., 66, No. 2, 209–219 (2016).
Popov, V. A., “Spontaneous potentiation of focal potentials in field CA1 in long-term living hippocampal slices from rats in the absence of electrical stimulation,” Zh. Vyssh. Nerv. Deyat., 44, No. 1, 149–158 (1994).
Prochnow, N., Abdulazim, A., Kurtenbach, S., et al., “Pannexin1 stabilizes synaptic plasticity and is needed for learning,” PLoS One, 7, No. 12, e51767 (2012).
Qiu, F., “Regulation of pannexin 1 channels by ATP,” Open Access Dissert., 394 (2010).
Qiu, F., Wang, J., and Dahl, G., “Alanine substitution scanning of pannexin1 reveals amino acid residues mediating ATP sensitivity,” Purinergic Signal, 8, 81–90 (2012).
Reymann, K. G., “Mechanisms underlying synaptic long-term potentiation in the hippocampus: focus on postsynaptic glutamate receptors and protein kinases,” Funct. Neurol. Suppl., 8, No. 5, 7–32 (1993).
Reymann, K. G., Frey, U., Jork, R., and Matthies, H., “Polymyxin B, an inhibitor of protein kinase C, prevents the maintenance of synaptic long-term potentiation in hippocampal CA1 neurons,” Brain Res., 440, No. 2, 305–314 (1988).
Rooney, T. A., Sass, E. J., and Thomas, A. P., “Agonist-induced cytosolic calcium oscillations originate from a specific locus in single hepatocytes,” J. Biol. Chem., 265, No. 18, 10,792–10,796 (1990).
Sosinsky, G. E., Boassa, D., Dermietzel, R., et al., “Pannexin channels are not gap junction hemichannels,” Channels (Austin), 5, No. 3, 193–197 (2011).
Storm, J. F., “Action potential repolarization and a fast after-hyperpolarization in rat hippocampal pyramidal cells,” J. Physiol., 385, 733–759 (1987).
Thompson, R. J., Jackson, M. F., Olah, M. E., et al., “Activation of pannexin-1 hemichannels augments aberrant bursting in the hippocampus,” Science, 322, 1555–1559 (2008).
Veech, R. L., Lawson, J. W. R., Cornell, N. W., and Krebs, H. A., “Cytosolic phosphorylation potential,” J. Biol. Chem., 254, No. 14, 6538–6547 (1979).
Weickert, S., Ray, A., Zoidl, G., and Dermietzel, R., “Expression of neural connexins and pannexin1 in the hippocampus and inferior olive: a quantitative approach,” Mol. Brain Res., 133, 102–109 (2005).
Zhao, H.-B., “Expression and function of pannexins in the inner ear and hearing,” BMC Cell Biol., 17, Supplement 1, 16 (2016).
Zoidl, G., Petrasch-Parwez, E., Ray, A., et al., “Localization of the pannexin1 protein at postsynaptic sites in the cerebral cortex and hippocampus,” Neuroscientist, 146, No. 1, 9–16 (2007).
Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 70, No. 3, pp. 360–374, May–June, 2020.
About this article
Cite this article
Popov, V.A. Involvement of Pannexin-1 in the Mechanism of Deprivation Potentiation of Population Spikes of Neurons in Rat Hippocampal Field CA1. Neurosci Behav Physi 51, 48–58 (2021). https://doi.org/10.1007/s11055-020-01038-2
- deprivation potentiation
- hippocampal slices
- pop spike
- input specificity
- P2 purine receptors