Dentate granule cell recruitment of feedforward inhibition governs engram maintenance

Jasnow, A.M., Lynch, J.F. III., Gilman, T.L. Riccio, D.C. Perspectives on fear generalization and its implications for emotional disorders. J. Neurosci. Res. 95, 821–835 (2017).

Biedenkapp, J.C. Rudy, J. W. Context pre-exposure prevents forgetting of a contextual fear memory: implication for regional changes in brain activation patterns associated with recent and remote memory tests. Learn. Mem. 14, 200–203 (2007).

Wiltgen, B.J. Silva, A.J. Memory for context becomes less specific with time. Learn. Mem. 14, 313–317 (2007).

Poulos, A.M. et al. Conditioning- and time-dependent increases in context fear and generalization. Learn. Mem. 23, 379–385 (2016).

Besnard, A. Sahay, A. Adult hippocampal neurogenesis, fear generalization and stress. Neuropsychopharmacology 41, 24–44 (2016).

Liberzon, I. Abelson, J.L. Context processing and the neurobiology of post-traumatic stress disorder. Neuron 92, 14–30 (2016).

Jovanovic, T. Ressler, K.J. How the neurocircuitry and genetics of fear inhibition may inform our understanding of PTSD. Am. J. Psychiatry 167, 648–662 (2010).

Leal, S.L. Yassa, M.A. Neurocognitive aging and the hippocampus across species. Trends Neurosci. 38, 800–812 (2015).

Bakker, A. et al. Reduction of hippocampal hyperactivity improves cognition in amnestic mild cognitive impairment. Neuron 74, 467–474 (2012).

Xu, W. Südhof, T.C. A neural circuit for memory specificity and generalization. Science 339, 1290–1295 (2013).

Ruediger, S. et al. Learning-related feedforward inhibitory connectivity growth required for memory precision. Nature 473, 514–518 (2011).

Kheirbek, M.A., Klemenhagen, K.C., Sahay, A. Hen, R. Neurogenesis and generalization: a new approach to stratify and treat anxiety disorders. Nat. Neurosci. 15, 1613–1620 (2012).

Likhtik, E., Stujenske, J.M., Topiwala, M.A., Harris, A.Z. Gordon, J.A. Prefrontal entrainment of amygdala activity signals safety in learned fear and innate anxiety. Nat. Neurosci. 17, 106–113 (2014).

Jones, G.L. et al. A genetic link between discriminative fear coding by the lateral amygdala, dopamine and fear generalization. eLife 4, e08969 (2015).

Lynch, J.F., Winiecki, P., Gilman, T.L., Adkins, J.M. Jasnow, A.M. Hippocampal GABAB(1a) receptors constrain generalized contextual fear. Neuropsychopharmacology 42, 914–924 (2017).

McClelland, J.L., McNaughton, B.L. O’Reilly, R.C. Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol. Rev. 1
, 419–457 (1995)

Frankland, P.W. Bontempi, B. The organization of recent and remote memories. Nat. Rev. Neurosci. 6, 119–130 (2005).

Winocur, G., Moscovitch, M. Sekeres, M. Memory consolidation or transformation: context manipulation and hippocampal representations of memory. Nat. Neurosci. 10, 555–557 (2007).

Wiltgen, B.J. et al. The hippocampus plays a selective role in the retrieval of detailed contextual memories. Curr. Biol. 20, 1336–1344 (2010).

Winocur, G., Moscovitch, M. Bontempi, B. Memory formation and long-term retention in humans and animals: convergence towards a transformation account of hippocampal–neocortical interactions. Neuropsychologia 48, 2339–2356 (2010).

Teyler, T.J. Rudy, J.W. The hippocampal indexing theory and episodic memory: updating the index. Hippocampus 17, 1158–1169 (2007).

Hardt, O., Nader, K. Nadel, L. Decay happens: the role of active forgetting in memory. Trends Cogn. Sci. 17, 111–120 (2013).

Frankland, P.W., Bontempi, B., Talton, L.E., Kaczmarek, L. Silva, A.J. The involvement of the anterior cingulate cortex in remote contextual fear memory. Science 304, 881–883 (2004).

Liu, X. et al. Identification and manipulation of memory engram cells. Cold Spring Harb. Symp. Quant. Biol. 79, 59–65 (2014).

Kitamura, T. et al. Engrams and circuits crucial for systems consolidation of a memory. Science 356, 73–78 (2017).

Acsády, L., Kamondi, A., Sík, A., Freund, T. Buzsáki, G. GABAergic cells are the major postsynaptic targets of mossy fibers in the rat hippocampus. J. Neurosci. 18, 3386–3403 (1998).

Martin, E.A. et al. The intellectual disability gene Kirrel3 regulates target-specific mossy fiber synapse development in the hippocampus. eLife 4, e09395 (2015).

Torborg, C.L., Nakashiba, T., Tonegawa, S. McBain, C.J. Control of CA3 output by feedforward inhibition despite developmental changes in the excitation–inhibition balance. J. Neurosci. 30, 15628–15637 (2010).

Mori, M., Abegg, M.H., Gähwiler, B.H. Gerber, U. A frequency-dependent switch from inhibition to excitation in a hippocampal unitary circuit. Nature 431, 453–456 (2004).

Porro, F. et al. β-adducin (Add2) KO mice show synaptic plasticity, motor coordination and behavioral deficits accompanied by changes in the expression and phosphorylation levels of the α- and γ-adducin subunits. Genes Brain Behav. 9, 84–96 (2010).

Rabenstein, R.L. et al. Impaired synaptic plasticity and learning in mice lacking β-adducin, an actin-regulating protein. J. Neurosci. 25, 2138–2145 (2005).

Buzsáki, G. Hippocampal sharp wave-ripple: a cognitive biomarker for episodic memory and planning. Hippocampus 25, 1073–1188 (2015).

Gan, J. et al. Phase-locked inhibition, but not excitation, underlies hippocampal ripple oscillations in awake mice in vivo. Neuron 93, 308–314 (2017).

Jadhav, S.P., Kemere, C., German, P.W. Frank, L.M. Awake hippocampal sharp-wave ripples support spatial memory. Science 336, 1454–1458 (2012).

Ognjanovski, N. et al. Parvalbumin-expressing interneurons coordinate hippocampal network dynamics required for memory consolidation. Nat. Commun. 8, 15039 (2017).

Nakashiba, T., Buhl, D.L., McHugh, T.J. Tonegawa, S. Hippocampal CA3 output is crucial for ripple-associated reactivation and consolidation of memory. Neuron 62, 781–787 (2009).

Çaliskan, G. et al. Identification of parvalbumin interneurons as cellular substrate of fear memory persistence. Cereb. Cortex 26, 2325–2340 (2016).

Wilson, I.A., Ikonen, S., Gallagher, M., Eichenbaum, H. Tanila, H. Age-associated alterations of hippocampal place cells are subregion specific. J. Neurosci. 25, 6877–6886 (2005).

Yassa, M.A. et al. Pattern separation deficits associated with increased hippocampal CA3 and dentate gyrus activity in nondemented older adults. Hippocampus 21, 968–979 (2011).

Simkin, D. et al. Aging-related hyperexcitability in CA3 pyramidal neurons is mediated by enhanced A-type K+ channel function and expression. J. Neurosci. 35, 13206–13218 (2015).

Thomé, A., Gray, D.T., Erickson, C.A., Lipa, P. Barnes, C.A. Memory impairment in aged primates is associated with region-specific network dysfunction. Mol. Psychiatry 21, 1257–1262 (2016).

Villanueva-Castillo, C., Tecuatl, C., Herrera-López, G. Galván, E.J. Aging-related impairments of hippocampal mossy fibers synapses on CA3 pyramidal cells. Neurobiol. Aging 49, 119–137 (2017).

Geinisman, Y., deToledo-Morrell, L., Morrell, F., Persina, I.S. Rossi, M. Age-related loss of axospinous synapses formed by two afferent systems in the rat dentate gyrus as revealed by the unbiased stereological dissector technique. Hippocampus 2, 437–444 (1992).

Reijmers, L.G., Perkins, B.L., Matsuo, N. Mayford, M. Localization of a stable neural correlate of associative memory. Science 317, 1230–1233 (2007).

Scobie, K.N. et al. Krüppel-like factor 9 is necessary for late-phase neuronal maturation in the developing dentate gyrus and during adult hippocampal neurogenesis. J. Neurosci. 29, 9875–9887 (2009).

Lundquist, E.A., Herman, R.K., Shaw, J.E. Bargmann, C.I. UNC-115, a conserved protein with predicted LIM and actin-binding domains, mediates axon guidance in C. elegans. Neuron 21, 385–392 (1998).

Barrientos, T. et al. Two novel members of the ABLIM protein family, ABLIM-2 and -3, associate with STARS and directly bind F-actin. J. Biol. Chem. 282, 8393–8403 (2007).

Matsuda, M., Yamashita, J.K., Tsukita, S.
Furuse, M. ABLIM3 is a novel component of adherens junctions with actin-binding activity. Eur. J. Cell Biol. 89, 807–816 (2010).

Cao, J. et al. miR-129-3p controls cilia assembly by regulating CP110 and actin dynamics. Nat. Cell Biol. 14, 697–706 (2012).

Beier, K.T. et al. Anterograde or retrograde trans-synaptic labeling of CNS neurons with vesicular stomatitis virus vectors. Proc. Natl. Acad. Sci. USA 108, 15414–15419 (2011).

Kamiya, H., Shinozaki, H. Yamamoto, C. Activation of metabotropic glutamate receptor type 2/3 suppresses transmission at rat hippocampal mossy fiber synapses. J. Physiol. (Lond.) 493, 447–455 (1996).

Liu, X. et al. Optogenetic stimulation of a hippocampal engram activates fear memory recall. Nature 484, 381–385 (2012).

Goshen, I. et al. Dynamics of retrieval strategies for remote memories. Cell 147, 678–689 (2011).

Vazdarjanova, A. McGaugh, J.L. Basolateral amygdala is involved in modulating consolidation of memory for classical fear conditioning. J. Neurosci. 19, 6615–6622 (1999).

Redondo, R.L. et al. Bidirectional switch of the valence associated with a hippocampal contextual memory engram. Nature 513, 426–430 (2014).

Girardeau, G., Inema, I. Buzsáki, G. Reactivations of emotional memory in the hippocampus–amygdala system during sleep. Nat. Neurosci. 20, 1634–1642 (2017).

Yang, C. Svitkina, T. Filopodia initiation: focus on the Arp2–3 complex and formins. Cell Adh. Migr. 5, 402–408 (2011).

Mejillano, M.R. et al. Lamellipodial versus filopodial mode of the actin nanomachinery: pivotal role of the filament barbed end. Cell 118, 363–373 (2004).

Wilson, M.A. McNaughton, B.L. Reactivation of hippocampal ensemble memories during sleep. Science 265, 676–679 (1994).

Bartos, M., Alle, H. Vida, I. Role of microcircuit structure and input integration in hippocampal interneuron recruitment and plasticity. Neuropharmacology 60, 730–739 (2011).

Zhou, Z. et al. Brain-specific phosphorylation of MeCP2 regulates activity-dependent Bdnf transcription, dendritic growth and spine maturation. Neuron 52, 255–269 (2006).

Lois, C., Hong, E.J., Pease, S., Brown, E.J. Baltimore, D. Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 295, 868–872 (2002).

Drokhlyansky, E. et al. The brain parenchyma has a type I interferon response that can limit virus spread. Proc. Natl. Acad. Sci. USA 114, E95–E104 (2017).

McAvoy, K.M. et al. Modulating neuronal competition dynamics in the dentate gyrus to rejuvenate aging memory circuits. Neuron 91, 1356–1373 (2016).

Ikrar, T. et al. Adult neurogenesis modifies excitability of the dentate gyrus. Front. Ne ural Circuits 7, 204 (2013).

Leave a Reply

Your email address will not be published. Required fields are marked *