AUTHOR CONTRIBUTIONS
G.C. performed electrophysiological experiments, analysed data and wrote the first draft of the manuscript; Y.E.D. contributed substantially to the analysis and presentation of the immunohistochemistry data; O.S. and G.C. conceptualized the study and wrote the manuscript. All authors confirmed the last version of the manuscript.
References
Åhlgren, J. & Voikar, V. (2019) Housing mice in the individually ventilated or open cages—Does it matter for behavioral phenotype?Genes, Brain Behav. , 18 , 1–12.
Albrecht, A., Çalişkan, G., Oitzl, M.S., Heinemann, U., & Stork, O. (2013) Long-lasting increase of corticosterone after fear memory reactivation: Anxiolytic effects and network activity modulation in the ventral hippocampus. Neuropsychopharmacology , 38 .
Antonoudiou, P., Tan, Y.L., Kontou, G., Upton, A.L., & Mann, E.O. (2020) Parvalbumin and Somatostatin Interneurons Contribute to the Generation of Hippocampal Gamma Oscillations. J. Neurosci. ,40 , 7668–7687.
Avshalom, C., Hariri, A.R., Andrew, H., Uher, R., & Moffitt, T.E. (2010) Genetic sensitivity to the environment: The case of the serotonin transporter gene and its implications for studying complex diseases and traits. Am. J. Psychiatry , 167 , 509–527.
Bazelot, M., Dinocourt, C., Cohen, I., & Miles, R. (2010) Unitary inhibitory field potentials in the CA3 region of rat hippocampus.J. Physiol. , 588 , 2077–2090.
Bazelot, M., Teleńczuk, M.T., & Miles, R. (2016) Single CA3 pyramidal cells trigger sharp waves in vitro by exciting interneurones. J. Physiol. , 594 , 2565–2577.
Behrens, C.J., van den Boom, L.P., de Hoz, L., Friedman, A., & Heinemann, U. (2005) Induction of sharp wave-ripple complexes in vitro and reorganization of hippocampal networks. Nat. Neurosci. ,8 , 1560–1567.
Beyeler, A., Retailleau, A., Molter, C., Mehidi, A., Szabadics, J., & Leinekugel, X. (2013) Recruitment of Perisomatic Inhibition during Spontaneous Hippocampal Activity In Vitro. PLoS One , 8 .
Bryant, C.D., Zhang, N.N., Sokoloff, G., Fanselow, M.S., Ennes, H.S., Palmer, A.A., & McRoberts, J.A. (2008) Behavioral differences among C57BL/6 substrains: Implications for transgenic and knockout studies.J. Neurogenet. , 22 , 315–331.
Butler, J.L. & Paulsen, O. (2015) Hippocampal network oscillations — recent insights from in vitro experiments. Curr. Opin. Neurobiol. , 31 , 40–44.
Buzsaki, G. (1989) Two-stage model of memory trace formation: A role for “noisy” brain states. Neuroscience , 31 , 551–570.
Buzsáki, G., Horváth, Z., Urioste, R., Hetke, J., & Wise, K. (1992) High-frequency network oscillation in the hippocampus. Science ,256 , 1025–1027.
Buzsáki, G. & Watson, B.O. (2012) Brain rhythms and neural syntax: implications for efficient coding of cognitive content and neuropsychiatric disease. Dialogues Clin. Neurosci. , 14 , 345–367.
Çalişkan, G., Müller, I., Semtner, M., Winkelmann, A., Raza, A.S., Hollnagel, J.O., Rösler, A., Heinemann, U., Stork, O., & Meier, J.C. (2016) Identification of Parvalbumin Interneurons as Cellular Substrate of Fear Memory Persistence. Cereb. Cortex , 26 , 2325–2340.
Caliskan, G., Schulz, S.B., Gruber, D., Behr, J., Heinemann, U., & Gerevich, Z. (2015) Corticosterone and corticotropin-releasing factor acutely facilitate gamma oscillations in the hippocampus in vitro.Eur. J. Neurosci. , 41 , 31–44.
Çalışkan, G., Albrecht, A., Hollnagel, J.O., Rösler, A., Richter-Levin, G., Heinemann, U., & Stork, O. (2015) Long-term changes in the CA3 associative network of fear-conditioned mice. Stress ,3890 , 1–32.
Çalışkan, G., Müller, I., Semtner, M., Winkelmann, A., Raza, A.S., Hollnagel, J.O., Rösler, A., Heinemann, U., Stork, O., & Meier, J.C. (2016) Identification of Parvalbumin Interneurons as Cellular Substrate of Fear Memory Persistence. Cereb. Cortex , 26 , 2325–2340.
Çalışkan, G. & Stork, O. (2018) Hippocampal network oscillations as mediators of behavioural metaplasticity: Insights from emotional learning. Neurobiol. Learn. Mem. , 154 , 37–53.
Camp, M., Norcross, M., Whittle, N., Feyder, M., D’Hanis, W., Yilmazer-Hanke, D., Singewald, N., & Holmes, A. (2009) Impaired Pavlovian fear extinction is a common phenotype across genetic lineages of the 129 inbred mouse strain. Genes, Brain Behav. , 8 , 744–752.
Camp, M.C., MacPherson, K.P., Lederle, L., Graybeal, C., Gaburro, S., Debrouse, L.M., Ihne, J.L., Bravo, J.A., O’Connor, R.M., Ciocchi, S., Wellman, C.L., Lüthi, A., Cryan, J.F., Singewald, N., & Holmes, A. (2012) Genetic strain differences in learned fear inhibition associated with variation in neuroendocrine, autonomic, and amygdala dendritic phenotypes. Neuropsychopharmacology , 37 , 1534–1547.
Contet, C., Rawlins, J.N.P., & Deacon, R.M.J. (2001) A comparison of 129S2/SvHsd and C57BL/6JOlaHsd mice on a test battery assessing sensorimotor, affective and cognitive behaviours: Implications for the study of genetically modified mice. Behav. Brain Res. ,124 , 33–46.
Csicsvari, J., Hirase, H., Mamiya, a, & Buzsáki, G. (2000) Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave-associated population events. Neuron , 28 , 585–594.
Deary, I.J., Johnson, W., & Houlihan, L.M. (2009) Genetic foundations of human intelligence. Hum. Genet. , 126 , 215–232.
Dunkley, B.T., Doesburg, S.M., Jetly, R., Sedge, P.A., Pang, E.W., & Taylor, M.J. (2015) Characterising intra- and inter-intrinsic network synchrony in combat-related post-traumatic stress disorder.Psychiatry Res. Neuroimaging , 234 , 172–181.
Dunkley, B.T., Doesburg, S.M., Sedge, P.A., Grodecki, R.J., Shek, P.N., Pang, E.W., & Taylor, M.J. (2014) Resting-state hippocampal connectivity correlates with symptom severity in post-traumatic stress disorder. NeuroImage Clin. , 5 , 377–384.
Ellender, T.J., Nissen, W., Colgin, L.L., Mann, E.O., & Paulsen, O. (2010) Priming of hippocampal population bursts by individual perisomatic-targeting interneurons. J. Neurosci. , 30 , 5979–5991.
Fano, S., Çalişkan, G., & Heinemann, U. (2012) Differential effects of blockade of ERG channels on gamma oscillations and excitability in rat hippocampal slices. Eur. J. Neurosci. , 36 .
Fanselow, M.S. & Dong, H.W. (2010) Are the Dorsal and Ventral Hippocampus Functionally Distinct Structures? Neuron ,65 , 7–19.
Fisahn, A., Pike, F.G., Buhl, E.H., & Paulsen, O. (1998) Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro.Nature , 394 , 186–189.
Freund, R.K., Graw, S., Choo, K.S., Stevens, K.E., Leonard, S., & Dell’Acqua, M.L. (2016) Genetic knockout of the α7 nicotinic acetylcholine receptor gene alters hippocampal long-term potentiation in a background strain-dependent manner. Neurosci. Lett. ,627 , 1–6.
Fries, P., Reynolds, J.H., Rorie, a E., & Desimone, R. (2001) Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention. Science (80-. ). , 291 , 1560–1563.
Gerlai, R. (1998a) A new continuous alternation task in T-maze detects hippocampal dysfunction in mice: A strain comparison and lesion study.Behav. Brain Res. , 95 , 91–101.
Gerlai, R. (1998b) Contextual learning and cue association in fear conditioning in mice: a strain comparison and a lesion study.Behav. Brain Res. , 95 , 191–203.
Gerlai, R. (2002) Hippocampal LTP and memory in mouse strains: Is there evidence for a causal relationship? Hippocampus , 12 , 657–666.
Girardeau, G., Benchenane, K., Wiener, S.I., Buzsáki, G., & Zugaro, M.B. (2009) Selective suppression of hippocampal ripples impairs spatial memory. Nat. Neurosci. , 12 , 1222–1223.
Girardeau, G., Inema, I., & Buzsáki, G. (2017) Reactivations of emotional memory in the hippocampus–amygdala system during sleep.Nat. Neurosci. , 20 , 1634–1642.
Gulyás, A.I., Szabó, G.G., Ulbert, I., Holderith, N., Monyer, H., Erdélyi, F., Szabó, G., Freund, T.F., & Hájos, N. (2010) Parvalbumin-containing fast-spiking basket cells generate the field potential oscillations induced by cholinergic receptor activation in the hippocampus. J. Neurosci. , 30 , 15134–15145.
Guyon, N., Zacharias, L.R., de Oliveira, E.F., Kim, H., Leite, J.P., Lopes-Aguiar, C., & Carlén, M. (2021) Network asynchrony underlying increased broadband gamma power. J. Neurosci. , JN-RM-2250-20.
Hajos, N., Karlocai, M.R., Nemeth, B., Ulbert, I., Monyer, H., Szabo, G., Erdelyi, F., Freund, T.F., & Gulyas, A.I. (2013) Input-Output Features of Anatomically Identified CA3 Neurons during Hippocampal Sharp Wave/Ripple Oscillation In Vitro. J. Neurosci. , 33 , 11677–11691.
Hájos, N., Pálhalini, J., Mann, E.O., Nèmeth, B., Paulsen, O., & Freund, T.F. (2004) Spike timing of distinct types of GABAergic interneuron during hippocampal gamma oscillations in vitro. J. Neurosci. , 24 , 9127–9137.
Hájos, N. & Paulsen, O. (2009) Network mechanisms of gamma oscillations in the CA3 region of the hippocampus. Neural Networks ,22 , 1113–1119.
Headley, D.B. & Paré, D. (2013) In sync: gamma oscillations and emotional memory. Front. Behav. Neurosci. , 7 , 170.
Heistek, T.S., Timmerman, A.J., Spijker, S., Brussaard, A.B., & Mansvelder, H.D. (2010) Gabaergic synapse properties may explain genetic variation in hippocampal network oscillations in mice. Front. Cell. Neurosci. , 4 , 1–11.
Jansen, R., Linkenkaer-Hansen, K., Heistek, T., Timmerman, J., Mansvelder, H.D., Brussaard, A.B., De Gunst, M., & Van Ooyen, A. (2009) Inbred mouse strains differ in multiple hippocampal activity traits.Eur. J. Neurosci. , 30 , 1092–1100.
Kjelstrup, K.G., Tuvnes, F.A., Steffenach, H.-A., Murison, R., Moser, E.I., & Moser, M.-B. (2002) Reduced fear expression after lesions of the ventral hippocampus. Proc. Natl. Acad. Sci. , 99 , 10825–10830.
Kudrimoti, H.S., Barnes, C.A., & McNaughton, B.L. (1999) Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J. Neurosci. , 19 , 4090–4101.
Le Duigou, C., Simonnet, J., Teleñczuk, M.T., Fricker, D., & Miles, R. (2014) Recurrent synapses and circuits in the CA3 region of the hippocampus: an associative network. Front. Cell. Neurosci. ,7 , 1–13.
Li, X.-G., Somogyi, P., Ylinen, A., & Buzsaki, G. (1994) The hippocampal CA3 network: An in vivo intracellularly labeling study.J. Comp. Neurol. , 339 , 181–208.
Lu, C.B., Jefferys, J.G.R., Toescu, E.C., & Vreugdenhil, M. (2011) In vitro hippocampal gamma oscillation power as an index of in vivo CA3 gamma oscillation strength and spatial reference memory.Neurobiol. Learn. Mem. , 95 , 221–230.
Madencioglu, D.A., Çalışkan, G., Yuanxiang, P., Rehberg, K., Demiray, Y.E., Kul, E., Engler, A., Hayani, H., Bergado-Acosta, J.R., Kummer, A., Müller, I., Song, I., Dityatev, A., Kähne, T., Kreutz, M.R., & Stork, O. (2021) Transgenic modeling of Ndr2 gene amplification reveals disturbance of hippocampus circuitry and function. iScience ,24 , 102868.
Maier, N., Nimmrich, V., & Draguhn, A. (2003) Cellular and network mechanisms underlying spontaneous sharp wave-ripple complexes in mouse hippocampal slices. J. Physiol. , 550 , 873–887.
Mann, E.O., Suckling, J.M., Hajos, N., Greenfield, S.A., & Paulsen, O. (2005) Perisomatic feedback inhibition underlies cholinergically induced fast network oscillations in the rat hippocampus in vitro.Neuron , 45 , 105–117.
March, A., Borchelt, D., Golde, T., & Janus, C. (2014) Differences in memory development among C57BL/6NCrl, 129S2/SvPasCrl, and FVB/NCrl mice after delay and trace fear conditioning. Comp. Med. , 64 , 4–12.
Maslarova, A., Lippmann, K., Salar, S., R??sler, A., & Heinemann, U. (2015) Differential participation of pyramidal cells in generation of spontaneous sharp wave-ripples in the mouse subiculum in vitro.Neurobiol. Learn. Mem. , 125 , 113–119.
Mizunuma, M., Norimoto, H., Tao, K., Egawa, T., Hanaoka, K., Sakaguchi, T., Hioki, H., Kaneko, T., Yamaguchi, S., Nagano, T., Matsuki, N., & Ikegaya, Y. (2014) Unbalanced excitability underlies offline reactivation of behaviorally activated neurons. Nat. Neurosci. ,17 , 503–505.
Montgomery, S.M. & Buzsáki, G. (2007) Gamma oscillations dynamically couple hippocampal CA3 and CA1 regions during memory task performance.Proc. Natl. Acad. Sci. U. S. A. , 104 , 14495–14500.
Müller, C. & Remy, S. (2014) Dendritic inhibition mediated by O-LM and bistratified interneurons in the hippocampus. Front. Synaptic Neurosci. , 6 , 1–15.
Nguyen, P. V., Abel, T., Kandel, E.R., & Bourtchouladze, R. (2000) Strain-dependent Differences in LTP and Hippocampus-dependent Memory in Inbred Mice. Learn. Mem. , 7 , 170–179.
Nguyen, P. V., Duffy, S.N., & Young, J.Z. (2000) Differential Maintenance and Frequency-Dependent Tuning of LTP at Hippocampal Synapses of Specific Strains of Inbred Mice. J. Neurophysiol. ,84 , 2484–2493.
Norimoto, H., Makino, K., Gao, M., Shikano, Y., Okamoto, K., Ishikawa, T., Sasaki, T., Hioki, H., Fujisawa, S., & Ikegaya, Y. (2018) Hippocampal ripples down-regulate synapses. Science (80-. ). ,359 , 1524–1527.
Ognjanovski, N., Schaeffer, S., Wu, J., Mofakham, S., Maruyama, D., Zochowski, M., & Aton, S.J. (2017) Parvalbumin-expressing interneurons coordinate hippocampal network dynamics required for memory consolidation. Nat. Commun. , 8 , 15039.
Oren, I., Mann, E.O., Paulsen, O., & Hájos, N. (2006) Synaptic currents in anatomically identified CA3 neurons during hippocampal gamma oscillations in vitro. J. Neurosci. , 26 , 9923–9934.
Pangalos, M., Donoso, J.R., Winterer, J., Zivkovic, A.R., Kempter, R., Maier, N., & Schmitz, D. (2013) Recruitment of oriens-lacunosum-moleculare interneurons during hippocampal ripples.Proc. Natl. Acad. Sci. U. S. A. , 110 , 4398–4403.
Radulovic, J., Kammermeier, J., & Spiess, J. (1998) Generalization of fear responses in C57BL/6N mice subjected to one- trial foreground contextual fear conditioning. Behav. Brain Res. , 95 , 179–189.
Ressler, K.J., Mercer, K.B., Bradley, B., Jovanovic, T., Mahan, A., Kerley, K., Norrholm, S.D., Kilaru, V., Smith, A.K., Myers, A.J., Ramirez, M., Engel, A., Hammack, S.E., Toufexis, D., Braas, K.M., Binder, E.B., & May, V. (2011) Post-traumatic stress disorder is associated with PACAP and the PAC1 receptor. Nature ,470 , 492–497.
Rodgers, R.J., Davies, B., & Shore, R. (2002) Absence of anxiolytic response to chlordiazepoxide in two common background strains exposed to the elevated plus-maze: Importance and implications of behavioural baseline. Genes, Brain Behav. , 1 , 242–251.
Savanthrapadian, S., Meyer, T., Elgueta, C., Booker, S.A., Vida, I., & Bartos, M. (2014) Synaptic properties of SOM-and CCK-expressing cells in dentate gyrus interneuron networks. J. Neurosci. , 34 , 8197–8209.
Schimanski, L.A., Ali, D.W., Baker, G.B., & Nguyen, P. V. (2007) Impaired hippocampal LTP in inbred mouse strains can be rescued by β-adrenergic receptor activation. Eur. J. Neurosci. , 25 , 1589–1598.
Schlingloff, D., Kali, S., Freund, T.F., Hajos, N., & Gulyas, A.I. (2014) Mechanisms of Sharp Wave Initiation and Ripple Generation.J. Neurosci. , 34 , 11385–11398.
Siegmund, A., Langnaese, K., & Wotjak, C.T. (2005) Differences in extinction of conditioned fear in C57BL/6 substrains are unrelated to expression of ??-synuclein. Behav. Brain Res. , 157 , 291–298.
Sloin, H.E., Bikovski, L., Levi, A., Amber-Vitos, O., Katz, T., Spivak, L., Someck, S., Gattegno, R., Sivroni, S., Sjulson, L., & Stark, E. (2022) Hybrid Offspring of C57BL/6J Mice Exhibit Improved Properties for Neurobehavioral Research. eneuro , 9 , ENEURO.0221-22.2022.
Stark, E., Roux, L., Eichler, R., Senzai, Y., Royer, S., & Buzsáki, G. (2014) Pyramidal Cell-Interneuron Interactions Underlie Hippocampal Ripple Oscillations. Neuron , 83 , 467–480.
Stiedl, O., Radulovic, J., Lohmann, R., Birkenfeld, K., Palve, M., Kammermeier, J., Sananbenesi, F., & Spiess, J. (1999) Strain and substrain differences in context- and tone-dependent fear conditioning of inbred mice. Behav. Brain Res. , 104 , 1–12.
Strange, B.A., Witter, M.P., Lein, E.S., & Moser, E.I. (2014) Functional organization of the hippocampal longitudinal axis. Nat. Rev. Neurosci. , 15 , 655–669.
Stujenske, J.M., Likhtik, E., Topiwala, M.A., & Gordon, J.A. (2014) Fear and Safety Engage Competing Patterns of Theta-Gamma Coupling in the Basolateral Amygdala. Neuron , 83 , 919–933.
Temme, S.J., Bell, R.Z., Pahumi, R., & Murphy, G.G. (2014) Comparison of inbred mouse substrains reveals segregation of maladaptive fear phenotypes. Front. Behav. Neurosci. , 8 , 1–9.
Vandecasteele, M., Varga, V., Berényi, A., Papp, E., Barthó, P., Venance, L., Freund, T.F., & Buzsáki, G. (2014) Optogenetic activation of septal cholinergic neurons suppresses sharp wave ripples and enhances theta oscillations in the hippocampus. Proc. Natl. Acad. Sci. U. S. A. , 111 , 13535–13540.
Wang, D. V, Yau, H.-J., Broker, C.J., Tsou, J.-H., Bonci, A., & Ikemoto, S. (2015) Mesopontine median raphe regulates hippocampal ripple oscillation and memory consolidation. Nat. Neurosci. ,18 , 728–735.
Wilson, M.A. & McNaughton, B.L. (1994) Reactivation of hippocampal ensemble memories during sleep. Science (80-. ). , 265 , 676–679.
Ylinen, A., Bragin, A., Nádasdy, Z., Jandó, G., Szabó, I., Sik, A., & Buzsáki, G. (1995) Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms.J. Neurosci. , 15 , 30–46.
Zemankovics, R., Veres, J.M., Oren, I., & Hajos, N. (2013) Feedforward Inhibition Underlies the Propagation of Cholinergically Induced Gamma Oscillations from Hippocampal CA3 to CA1. J. Neurosci. ,33 , 12337–12351.