Somatosensory-Evoked Early Sharp Waves in the Neonatal Rat Hippocampus
Abstract
1. Introduction
2. Results
3. Discussion
4. Materials and Methods
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Conflicts of Interest
References
- Cossart, R.; Khazipov, R. How development sculpts hippocampal circuits and function. Physiol. Rev. 2022, 102, 343–378. [Google Scholar] [CrossRef]
- Leinekugel, X.; Khazipov, R.; Cannon, R.; Hirase, H.; Ben Ari, Y.; Buzsaki, G. Correlated bursts of activity in the neonatal hippocampus in vivo. Science 2002, 296, 2049–2052. [Google Scholar] [CrossRef]
- Marguet, S.L.; Le-Schulte, V.T.; Merseburg, A.; Neu, A.; Eichler, R.; Jakovcevski, I.; Ivanov, A.; Hanganu-Opatz, I.L.; Bernard, C.; Morellini, F.; et al. Treatment during a vulnerable developmental period rescues a genetic epilepsy. Nat. Med. 2015, 21, 1436–1444. [Google Scholar] [CrossRef]
- Mohns, E.J.; Blumberg, M.S. Synchronous bursts of neuronal activity in the developing hippocampus: Modulation by active sleep and association with emerging gamma and theta rhythms. J. Neurosci. 2008, 28, 10134–10144. [Google Scholar] [CrossRef]
- Mohns, E.J.; Karlsson, K.A.; Blumberg, M.S. Developmental emergence of transient and persistent hippocampal events and oscillations and their association with infant seizure susceptibility. Eur. J. Neurosci. 2007, 26, 2719–2730. [Google Scholar] [CrossRef] [PubMed]
- Valeeva, G.; Janackova, S.; Nasretdinov, A.; Rychkova, V.; Makarov, R.; Holmes, G.L.; Khazipov, R.; Lenck-Santini, P.P. Emergence of Coordinated Activity in the Developing Entorhinal-Hippocampal Network. Cereb. Cortex 2019, 29, 906–920. [Google Scholar] [CrossRef] [PubMed]
- Buzsaki, G. Hippocampal sharp wave-ripple: A cognitive biomarker for episodic memory and planning. Hippocampus 2015, 25, 1073–1188. [Google Scholar] [CrossRef]
- Karlsson, K.A.; Mohns, E.J.; di Prisco, G.V.; Blumberg, M.S. On the co-occurrence of startles and hippocampal sharp waves in newborn rats. Hippocampus 2006, 16, 959–965. [Google Scholar] [CrossRef]
- Leprince, E.; Dard, R.F.; Mortet, S.; Filippi, C.; Giorgi-Kurz, M.; Bourboulou, R.; Lenck-Santini, P.P.; Picardo, M.A.; Bocchio, M.; Baude, A.; et al. Extrinsic control of the early postnatal CA1 hippocampal circuits. Neuron 2023, 111, 888–902.e8. [Google Scholar] [CrossRef]
- Dard, R.F.; Leprince, E.; Denis, J.; Rao Balappa, S.; Suchkov, D.; Boyce, R.; Lopez, C.; Giorgi-Kurz, M.; Szwagier, T.; Dumont, T.; et al. The rapid developmental rise of somatic inhibition disengages hippocampal dynamics from self-motion. eLife 2022, 11, e78116. [Google Scholar] [CrossRef] [PubMed]
- Inacio, A.R.; Nasretdinov, A.; Lebedeva, J.; Khazipov, R. Sensory feedback synchronizes motor and sensory neuronal networks in the neonatal rat spinal cord. Nat. Commun. 2016, 7, 13060. [Google Scholar] [CrossRef] [PubMed]
- Petersson, P.; Waldenstrom, A.; Fahraeus, C.; Schouenborg, J. Spontaneous muscle twitches during sleep guide spinal self-organization. Nature 2003, 424, 72–75. [Google Scholar] [CrossRef]
- Akhmetshina, D.; Nasretdinov, A.; Zakharov, A.; Valeeva, G.; Khazipov, R. The Nature of the Sensory Input to the Neonatal Rat Barrel Cortex. J. Neurosci. 2016, 36, 9922–9932. [Google Scholar] [CrossRef] [PubMed]
- Dooley, J.C.; Glanz, R.M.; Sokoloff, G.; Blumberg, M.S. Self-Generated Whisker Movements Drive State-Dependent Sensory Input to Developing Barrel Cortex. Curr. Biol. 2020, 30, 2404–2410. [Google Scholar] [CrossRef] [PubMed]
- Khazipov, R.; Sirota, A.; Leinekugel, X.; Holmes, G.L.; Ben Ari, Y.; Buzsaki, G. Early motor activity drives spindle bursts in the developing somatosensory cortex. Nature 2004, 432, 758–761. [Google Scholar] [CrossRef]
- McVea, D.A.; Mohajerani, M.H.; Murphy, T.H. Voltage-sensitive dye imaging reveals dynamic spatiotemporal properties of cortical activity after spontaneous muscle twitches in the newborn rat. J. Neurosci. 2012, 32, 10982–10994. [Google Scholar] [CrossRef]
- Colonnese, M.T.; Kaminska, A.; Minlebaev, M.; Milh, M.; Bloem, B.; Lescure, S.; Moriette, G.; Chiron, C.; Ben-Ari, Y.; Khazipov, R. A conserved switch in sensory processing prepares developing neocortex for vision. Neuron 2010, 67, 480–498. [Google Scholar] [CrossRef]
- Khazipov, R.; Milh, M. Early patterns of activity in the developing cortex: Focus on the sensorimotor system. Semin. Cell Dev. Biol. 2018, 76, 120–129. [Google Scholar] [CrossRef]
- Khazipov, R.; Luhmann, H.J. Early patterns of electrical activity in the developing cerebral cortex of humans and rodents. Trends Neurosci. 2006, 29, 414–418. [Google Scholar] [CrossRef]
- Luhmann, H.J.; Khazipov, R. Neuronal activity patterns in the developing barrel cortex. Neuroscience 2018, 368, 256–267. [Google Scholar] [CrossRef]
- Mohns, E.J.; Blumberg, M.S. Neocortical activation of the hippocampus during sleep in infant rats. J. Neurosci. 2010, 30, 3438–3449. [Google Scholar] [CrossRef] [PubMed]
- Buzsaki, G.; Moser, E.I. Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat. Neurosci. 2013, 16, 130–138. [Google Scholar] [CrossRef] [PubMed]
- Bellistri, E.; Aguilar, J.; Brotons-Mas, J.R.; Foffani, G.; de la Prida, L.M. Basic properties of somatosensory-evoked responses in the dorsal hippocampus of the rat. J. Physiol. 2013, 591, 2667–2686. [Google Scholar] [CrossRef]
- Brankack, J.; Buzsaki, G. Hippocampal responses evoked by tooth pulp and acoustic stimulation: Depth profiles and effect of behavior. Brain Res. 1986, 378, 303–314. [Google Scholar] [CrossRef] [PubMed]
- Deadwyler, S.A.; West, M.O.; Robinson, J.H. Entorhinal and septal inputs differentially control sensory-evoked responses in the rat dentate gyrus. Science 1981, 211, 1181–1183. [Google Scholar] [CrossRef] [PubMed]
- O’Keefe, J.; Krupic, J. Do hippocampal pyramidal cells respond to nonspatial stimuli? Physiol. Rev. 2021, 101, 1427–1456. [Google Scholar] [CrossRef]
- Pereira, A.; Ribeiro, S.; Wiest, M.; Moore, L.C.; Pantoja, J.; Lin, S.C.; Nicolelis, M.A. Processing of tactile information by the hippocampus. Proc. Natl. Acad. Sci. USA 2007, 104, 18286–18291. [Google Scholar] [CrossRef]
- Vinogradova, O.S. Hippocampus as comparator: Role of the two input and two output systems of the hippocampus in selection and registration of information. Hippocampus 2001, 11, 578–598. [Google Scholar] [CrossRef]
- Valeeva, G.; Nasretdinov, A.; Rychkova, V.; Khazipov, R. Bilateral Synchronization of Hippocampal Early Sharp Waves in Neonatal Rats. Front. Cell. Neurosci. 2019, 13, 29. [Google Scholar] [CrossRef]
- Minlebaev, M.; Colonnese, M.; Tsintsadze, T.; Sirota, A.; Khazipov, R. Early gamma oscillations synchronize developing thalamus and cortex. Science 2011, 334, 226–229. [Google Scholar] [CrossRef]
- Tiriac, A.; Uitermarkt, B.D.; Fanning, A.S.; Sokoloff, G.; Blumberg, M.S. Rapid whisker movements in sleeping newborn rats. Curr. Biol. 2012, 22, 2075–2080. [Google Scholar] [CrossRef]
- Yang, J.W.; An, S.; Sun, J.J.; Reyes-Puerta, V.; Kindler, J.; Berger, T.; Kilb, W.; Luhmann, H.J. Thalamic Network Oscillations Synchronize Ontogenetic Columns in the Newborn Rat Barrel Cortex. Cereb. Cortex 2013, 23, 1299–1316. [Google Scholar] [CrossRef]
- Yang, J.W.; Hanganu-Opatz, I.L.; Sun, J.J.; Luhmann, H.J. Three patterns of oscillatory activity differentially synchronize developing neocortical networks in vivo. J. Neurosci. 2009, 29, 9011–9025. [Google Scholar] [CrossRef]
- Unichenko, P.; Yang, J.W.; Luhmann, H.J.; Kirischuk, S. Glutamatergic system controls synchronization of spontaneous neuronal activity in the murine neonatal entorhinal cortex. Pflug. Arch. 2015, 467, 1565–1575. [Google Scholar] [CrossRef]
- Bragin, A.; Jando, G.; Nadasdy, Z.; van Landeghem, M.; Buzsaki, G. Dentate EEG spikes and associated interneuronal population bursts in the hippocampal hilar region of the rat. J. Neurophysiol. 1995, 73, 1691–1705. [Google Scholar] [CrossRef] [PubMed]
- Doischer, D.; Hosp, J.A.; Yanagawa, Y.; Obata, K.; Jonas, P.; Vida, I.; Bartos, M. Postnatal differentiation of basket cells from slow to fast signaling devices. J. Neurosci. 2008, 28, 12956–12968. [Google Scholar] [CrossRef] [PubMed]
- Khazipov, R.; Minlebaev, M.; Valeeva, G. Early gamma oscillations. Neuroscience 2013, 250, 240–252. [Google Scholar] [CrossRef]
- Le, M.C.; Monyer, H. GABAergic interneurons shape the functional maturation of the cortex. Neuron 2013, 77, 388–405. [Google Scholar]
- Pelkey, K.A.; Chittajallu, R.; Craig, M.T.; Tricoire, L.; Wester, J.C.; McBain, C.J. Hippocampal GABAergic Inhibitory Interneurons. Physiol. Rev. 2017, 97, 1619–1747. [Google Scholar] [CrossRef]
- Ben Ari, Y.; Gaiarsa, J.L.; Tyzio, R.; Khazipov, R. GABA: A Pioneer Transmitter That Excites Immature Neurons and Generates Primitive Oscillations. Physiol. Rev. 2007, 87, 1215–1284. [Google Scholar] [CrossRef]
- Murata, Y.; Colonnese, M.T. GABAergic interneurons excite neonatal hippocampus in vivo. Sci. Adv. 2020, 6, eaba1430. [Google Scholar] [CrossRef] [PubMed]
- Graf, J.; Zhang, C.; Marguet, S.L.; Herrmann, T.; Flossmann, T.; Hinsch, R.; Rahmati, V.; Guenther, M.; Frahm, C.; Urbach, A.; et al. A limited role of NKCC1 in telencephalic glutamatergic neurons for developing hippocampal network dynamics and behavior. Proc. Natl. Acad. Sci. USA 2021, 118, e2014784118. [Google Scholar] [CrossRef] [PubMed]
- Donato, F.; Jacobsen, R.I.; Moser, M.B.; Moser, E.I. Stellate cells drive maturation of the entorhinal-hippocampal circuit. Science 2017, 355, eaai8178. [Google Scholar] [CrossRef] [PubMed]
- Kasyanov, A.M.; Safiulina, V.F.; Voronin, L.L.; Cherubini, E. GABA-mediated giant depolarizing potentials as coincidence detectors for enhancing synaptic efficacy in the developing hippocampus. Proc. Natl. Acad. Sci. USA 2004, 101, 3967–3972. [Google Scholar] [CrossRef]
- Durand, G.M.; Kovalchuk, Y.; Konnerth, A. Long-term potentiation and functional synapse induction in developing hippocampus. Nature 1996, 381, 71–75. [Google Scholar] [CrossRef] [PubMed]
- Groc, L.; Petanjek, Z.; Gustafsson, B.; Ben Ari, Y.; Hanse, E.; Khazipov, R. In vivo blockade of neural activity alters dendritic development of neonatal CA1 pyramidal cells. Eur. J. Neurosci. 2002, 16, 1931–1938. [Google Scholar] [CrossRef] [PubMed]
- Ben-Ari, Y.; Khazipov, R.; Leinekugel, X.; Caillard, O.; Gaïarsa, J.-L. GABAA, NMDA and AMPA receptors: A developmentally regulated ‘ménage a trois’. Trends Neurosci. 1997, 20, 523–529. [Google Scholar] [CrossRef] [PubMed]
- Leinekugel, X.; Medina, I.; Khalilov, I.; Ben-Ari, Y.; Khazipov, R. Ca2+ oscillations mediated by the synergistic excitatory actions of GABAA and NMDA receptors in the neonatal hippocampus. Neuron 1997, 18, 243–255. [Google Scholar] [CrossRef]
- Khazipov, R.; Zaynutdinova, D.; Ogievetsky, E.; Valeeva, G.; Mitrukhina, O.; Manent, J.B.; Represa, A. Atlas of the Postnatal Rat Brain in Stereotaxic Coordinates. Front. Neuroanat. 2015, 9, 161. [Google Scholar] [CrossRef]
- Freeman, J.A.; Nicholson, C. Experimental optimization of current source-density technique for anuran cerebellum. J. Neurophysiol. 1975, 38, 369–382. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Gainutdinov, A.; Shipkov, D.; Sintsov, M.; Fabrizi, L.; Nasretdinov, A.; Khazipov, R.; Valeeva, G. Somatosensory-Evoked Early Sharp Waves in the Neonatal Rat Hippocampus. Int. J. Mol. Sci. 2023, 24, 8721. https://doi.org/10.3390/ijms24108721
Gainutdinov A, Shipkov D, Sintsov M, Fabrizi L, Nasretdinov A, Khazipov R, Valeeva G. Somatosensory-Evoked Early Sharp Waves in the Neonatal Rat Hippocampus. International Journal of Molecular Sciences. 2023; 24(10):8721. https://doi.org/10.3390/ijms24108721
Chicago/Turabian StyleGainutdinov, Azat, Dmitrii Shipkov, Mikhail Sintsov, Lorenzo Fabrizi, Azat Nasretdinov, Roustem Khazipov, and Guzel Valeeva. 2023. "Somatosensory-Evoked Early Sharp Waves in the Neonatal Rat Hippocampus" International Journal of Molecular Sciences 24, no. 10: 8721. https://doi.org/10.3390/ijms24108721
APA StyleGainutdinov, A., Shipkov, D., Sintsov, M., Fabrizi, L., Nasretdinov, A., Khazipov, R., & Valeeva, G. (2023). Somatosensory-Evoked Early Sharp Waves in the Neonatal Rat Hippocampus. International Journal of Molecular Sciences, 24(10), 8721. https://doi.org/10.3390/ijms24108721