A cortical–hippocampal system for declarative memory. Nature Rev. Neurosci.
1, 41–50 (2000).
et al. The labile nature of consolidation theory. Nature Rev. Neurosci.
1, 216–219 (2000).
Schafe, G. E.
et al. Memory consolidation of Pavlovian fear conditioning: a cellular and molecular perspective. Trends Neurosci.
24, 540–546 (2001).
Bouton, M. E.
Context and behavioral processes in extinction. Learn. Mem.
11, 485–494 (2004).
Maren, S. & Quirk, G. J.
Neuronal signalling of fear memory. Nature Rev. Neurosci.
5, 844–852 (2004).
Fanselow, M. S. & Poulos, A. M.
The neuroscience of mammalian associative learning. Annu. Rev. Psychol.
56, 207–234 (2005).
McKenzie, S. & Eichenbaum, H.
Consolidation and reconsolidation: two lives of memories?
71, 224–233 (2011).
Silva, A. J.
et al. Molecular and cellular approaches to memory allocation in neural circuits. Science
326, 391–395 (2009). This review developed the hypothesis that a CREB-dependent increase in excitability is a mechanism by which memories are allocated and thereby linked in the brain.
Simple memory: a theory for archicortex. Phil. Trans. R. Soc. Lond. B
262, 23–81 (1971).
Simoncelli, E. P. & Olshausen, B. A.
Natural image statistics and neural representation. Annu. Rev. Neurosci.
24, 1193–1216 (2001).
Olshausen, B. A. & Field, D. J.
Sparse coding of sensory inputs. Curr. Opin. Neurobiol.
14, 481–487 (2004).
Quiroga, R. Q.
et al. Sparse but not 'grandmother-cell' coding in the medial temporal lobe. Trends Cogn. Sci.
12, 87–91 (2008).
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.
102, 419–457 (1995).
Hippocampus: cognitive processes and neural representations that underlie declarative memory. Neuron
44, 109–120 (2004).
Han, J. H.
et al. Neuronal competition and selection during memory formation. Science
316, 457–460 (2007). This paper shows that the levels of CREB in the lateral amygdala can modulate the probability that a given neuron will be involved in an auditory fear memory.
et al. CREB regulates excitability and the allocation of memory to subsets of neurons in the amygdala. Nature Neurosci.
12, 1438–1443 (2009). A study showing that CREB regulates neuronal excitability and therefore the probability that a given lateral amygdala neuron will be involved in tone conditioning and conditioned taste aversion.
Maren, S. & Fanselow, M. S.
The amygdala and fear conditioning: has the nut been cracked?
16, 237–240 (1996).
Repa, J. C.
et al. Two different lateral amygdala cell populations contribute to the initiation and storage of memory. Nature Neurosci.
4, 724–731 (2001).
Johansen, J. P.
et al. Neural substrates for expectation-modulated fear learning in the amygdala and periaqueductal gray. Nature Neurosci.
13, 979–986 (2010).
Quirk, G. J., Repa, C. & LeDoux, J. E.
Fear conditioning enhances short-latency auditory responses of lateral amygdala neurons: parallel recordings in the freely behaving rat. Neuron
15, 1029–1039 (1995).
et al. Postsynaptic receptor trafficking underlying a form of associative learning. Science
308, 83–88 (2005).
Reijmers, L. G.
et al. Localization of a stable neural correlate of associative memory. Science
317, 1230–1233 (2007).
Han, J. H.
et al. Selective erasure of a fear memory. Science
323, 1492–1496 (2009). The authors of this study ablated a set of neurons constituting a CREB-biased auditory fear memory trace and demonstrated that those neurons were needed for recall.
Tan, E. M.
et al. Selective and quickly reversible inactivation of mammalian neurons in vivo using the Drosophila allatostatin receptor. Neuron
51, 157–170 (2006).
et al. Blockade of stimulus convergence in amygdala neurons disrupts taste associative learning. J. Neurosci.
33, 4958–4963 (2013).
Frostig, R. D.
Functional organization and plasticity in the adult rat barrel cortex: moving out-of-the-box. Curr. Opin. Neurobiol.
16, 445–450 (2006).
et al. Vibrissa-signaled eyeblink conditioning induces somatosensory cortical plasticity. J. Neurosci.
26, 6062–6068 (2006).
et al. A novel method for precisely timed stimulation of mouse whiskers in a freely moving preparation: application for delivery of the conditioned stimulus in trace eyeblink conditioning. J. Neurosci. Methods
177, 434–439 (2009).
et al. Associative fear learning enhances sparse network coding in primary sensory cortex. Neuron
75, 121–132 (2012).
Ward, R. L.
et al. Infragranular barrel cortex activity is enhanced with learning. J. Neurophysiol.
108, 1278–1287 (2012).
Sekeres, M. J.
et al. Dorsal hippocampal CREB is both necessary and sufficient for spatial memory. Learn. Mem.
17, 280–283 (2010).
et al. Viral-mediated expression of a constitutively active form of CREB in hippocampal neurons increases memory. Hippocampus
19, 228–234 (2009).
Lopez de Armentia, M.
et al. cAMP response element-binding protein-mediated gene expression increases the intrinsic excitability of CA1 pyramidal neurons. J. Neurosci.
27, 13909–13918 (2007).
et al. Intracellular determinants of hippocampal CA1 place and silent cell activity in a novel environment. Neuron
70, 109–120 (2011).
et al. Hippocampal place fields emerge upon single-cell manipulation of excitability during behavior. Science
337, 849–853 (2012).
et al. CREB modulates excitability of nucleus accumbens neurons. Nature Neurosci.
9, 475–477 (2006).
Dragoi, G. & Tonegawa, S.
Preplay of future place cell sequences by hippocampal cellular assemblies. Nature
469, 397–401 (2011).
Choi, G. B.
et al. Driving opposing behaviors with ensembles of piriform neurons. Cell
146, 1004–1015 (2011).
Nestor, M. W. & Hoffman, D. A.
Aberrant dendritic excitability: a common pathophysiology in CNS disorders affecting memory?
45, 478–487 (2012).
Merzenich, M. M.
et al. Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation. Neuroscience
8, 33–55 (1983).
Asaad, W. F.
et al. Neural activity in the primate prefrontal cortex during associative learning. Neuron
21, 1399–1407 (1998).
Fuster, J. M.
et al. Cross-modal and cross-temporal association in neurons of frontal cortex. Nature
405, 347–351 (2000).
Garner, A. R.
et al. Generation of a synthetic memory trace. Science
335, 1513–1516 (2012). In this study, the authors created a synthetic memory trace derived from the conjunction of a context and an artificially activated ensemble of neurons.
et al. Creating a false memory in the hippocampus. Science
341, 387–391 (2013).
Howard, M. W. & Kahana, M. J.
A distributed representation of temporal context. J. Math. Psychol.
46, 269–299 (2002).
et al. Linking neuronal ensembles by associative synaptic plasticity. PLoS ONE
6, e20486 (2011).
et al. Dendritic coding of multiple sensory inputs in single cortical neurons in vivo. Proc. Natl Acad. Sci. USA
108, 15420–15425 (2011).
Abraham, W. C. & Bear, M. F.
Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci.
19, 126–130 (1996).
Mockett, B. G. & Hulme, S. R.
Metaplasticity: new insights through electrophysiological investigations. J. Integr. Neurosci.
7, 315–336 (2008).
Frey, U. & Morris, R. G.
Synaptic tagging: implications for late maintenance of hippocampal long-term potentiation. Trends Neurosci.
21, 181–188 (1998).
Redondo, R. L. & Morris, R. G.
Making memories last: the synaptic tagging and capture hypothesis. Nature Rev. Neurosci.
12, 17–30 (2011).
et al. Specific long-lasting potentiation of synaptic transmission in hippocampal slices. Nature
266, 736–737 (1977).
Lynch, G. S.
et al. Heterosynaptic depression: a postsynaptic correlate of long-term potentiation. Nature
266, 737–739 (1977).
Frey, U. & Morris, R. G.
Synaptic tagging and long-term potentiation. Nature
385, 533–536 (1997). This paper shows that a strong synaptic input creates a protein synthesis-independent synaptic tag at potentiated synapses that sequesters proteins needed for a late phase of a synaptic potentiation.
Frey, U. & Morris, R. G.
Weak before strong: dissociating synaptic tagging and plasticity-factor accounts of late-LTP. Neuropharmacology
37, 545–552 (1998).
Sajikumar, S. & Frey, J. U.
Late-associativity, synaptic tagging, and the role of dopamine during LTP and LTD. Neurobiol. Learn. Mem.
82, 12–25 (2004).
Martin, K. C.
et al. Synapse-specific, long-term facilitation of Aplysia sensory to motor synapses: a function for local protein synthesis in memory storage. Cell
91, 927–938 (1997).
et al. A transient, neuron-wide form of CREB-mediated long-term facilitation can be stabilized at specific synapses by local protein synthesis. Cell
99, 221–237 (1999).
Ramachandran, B. & Frey, J. U.
Interfering with the actin network and its effect on long-term potentiation and synaptic tagging in hippocampal CA1 neurons in slices in vitro. J. Neurosci.
29, 12167–12173 (2009).
Redondo, R. L.
et al. Synaptic tagging and capture: differential role of distinct calcium/calmodulin kinases in protein synthesis-dependent long-term potentiation. J. Neurosci.
30, 4981–4989 (2010).
Auerbach, J. M. & Segal, M.
A novel cholinergic induction of long-term potentiation in rat hippocampus. J. Neurophysiol.
72, 2034–2040 (1994).
et al. Brain-derived neurotrophic factor triggers transcription-dependent, late phase long-term potentiation in vivo. J. Neurosci.
22, 7453–7461 (2002).
et al. Synergistic requirements for the induction of dopaminergic D1/D5-receptor-mediated LTP in hippocampal slices of rat CA1 in vitro. Neuropharmacology
52, 1547–1554 (2007).
Harvey, C. D.
et al. The spread of Ras activity triggered by activation of a single dendritic spine. Science
321, 136–140 (2008). This study shows that LTP triggers biochemical changes that are shared by nearby synapses in the same dendrite and that this affects thresholds of LTP in these synapses.
Patterson, M. A., Szatmari, E. M. & Yasuda, R.
AMPA receptors are exocytosed in stimulated spines and adjacent dendrites in a Ras–ERK-dependent manner during long-term potentiation. Proc. Natl Acad. Sci. USA
107, 15951–15956 (2010).
Murakoshi, H., Wang, H. & Yasuda, R.
Local, persistent activation of Rho GTPases during plasticity of single dendritic spines. Nature
472, 100–104 (2011).
et al. The dendritic branch is the preferred integrative unit for protein synthesis-dependent LTP. Neuron
69, 132–146 (2011).
Govindarajan, A., Kelleher, R. J. & Tonegawa, S.
A clustered plasticity model of long-term memory engrams. Nature Rev. Neurosci.
7, 575–583 (2006).
Steward, O. & Schuman, E. M.
Protein synthesis at synaptic sites on dendrites. Annu. Rev. Neurosci.
24, 299–325 (2001).
Martin, K. C. & Kosik, K. S.
Synaptic tagging — who's it?
Nature Rev. Neurosci.
3, 813–820 (2002).
Frick, A. & Johnston, D.
Plasticity of dendritic excitability. J. Neurobiol.
64, 100–115 (2005).
Moncada, D. & Viola, H.
Induction of long-term memory by exposure to novelty requires protein synthesis: evidence for a behavioral tagging. J. Neurosci.
27, 7476–7481 (2007). This study uncovers interactions between memories that exhibit the defining features of the synaptic tagging and capture hypothesis.
et al. Behavioral tagging is a general mechanism of long-term memory formation. Proc. Natl Acad. Sci. USA
106, 14599–14604 (2009).
et al. Recognition memory for single tones with and without context. J. Exp. Psychol. Hum. Learn. Mem.
3, 60–67 (1977).
Wang, S. H.
et al. Relevance of synaptic tagging and capture to the persistence of long-term potentiation and everyday spatial memory. Proc. Natl Acad. Sci. USA
107, 19537–19542 (2010).
et al. Novelty causes time-dependent retrograde amnesia for one-trial avoidance in rats through NMDA receptor- and CaMKII-dependent mechanisms in the hippocampus. Eur. J. Neurosci.
11, 3323–3328 (1999).
Poirazi, P. & Mel, B. W.
Impact of active dendrites and structural plasticity on the memory capacity of neural tissue. Neuron
29, 779–796 (2001).
Losonczy, A. & Magee, J. C.
Integrative properties of radial oblique dendrites in hippocampal CA1 pyramidal neurons. Neuron
50, 291–307 (2006).
et al. Repetitive motor learning induces coordinated formation of clustered dendritic spines in vivo. Nature
483, 92–95 (2012). This paper shows that there is synaptic clustering of functionally related inputs in the motor cortex during a forelimb motor-learning task.
et al. Elimination of dendritic spines with long-term memory is specific to active circuits. J. Neurosci.
32, 12570–12578 (2012).
Lai, C. S.
et al. Opposite effects of fear conditioning and extinction on dendritic spine remodelling. Nature
483, 87–91 (2012).
Quirk, G. J. & Mueller, D.
Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology
33, 56–72 (2008).
et al. LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature
402, 421–425 (1999).
Nikonenko, I., Jourdain, P. & Muller, D.
Presynaptic remodeling contributes to activity-dependent synaptogenesis. J. Neurosci.
23, 8498–8505 (2003).
Tolias, K. F., Duman, J. G. & Um, K.
Control of synapse development and plasticity by Rho GTPase regulatory proteins. Prog. Neurobiol.
94, 133–148 (2011).
Larkum, M. E. & Nevian, T.
Synaptic clustering by dendritic signalling mechanisms. Curr. Opin. Neurobiol.
18, 321–331 (2008).
Losonczy, A., Makara, J. K. & Magee, J. C.
Compartmentalized dendritic plasticity and input feature storage in neurons. Nature
452, 436–441 (2008).
The Child's Conception of the World (Routledge, 1929).
Bartlett, F. C.
Remembering: A Study in Experimental and Social Psychology (Cambridge Univ. Press, 1932).
et al. Schema-dependent gene activation and memory encoding in neocortex. Science
333, 891–895 (2011). This study suggests that schema in the neocortex can account for the rapid acquisition and consolidation of related information.
et al. Schemas and memory consolidation. Science
316, 76–82 (2007).
et al. Learning causes reorganization of neuronal firing patterns to represent related experiences within a hippocampal schema. J. Neurosci.
33, 10243–10256 (2013).
et al. Identification of transmitter systems and learning tag molecules involved in behavioral tagging during memory formation. Proc. Natl Acad. Sci. USA
108, 12931–12936 (2011).
Zeithamova, D., Dominick, A. L. & Preston, A. R.
Hippocampal and ventral medial prefrontal activation during retrieval-mediated learning supports novel inference. Neuron
75, 168–179 (2012).
et al. Impaired phosphorylation of cyclic AMP response element binding protein in the hippocampus of dementia of the Alzheimer type. Brain Res.
824, 300–303 (1999).
Satoh, J., Tabunoki, H. & Arima, K.
Molecular network analysis suggests aberrant CREB-mediated gene regulation in the Alzheimer disease hippocampus. Dis. Markers
27, 239–252 (2009).
et al. CBP gene transfer increases BDNF levels and ameliorates learning and memory deficits in a mouse model of Alzheimer's disease. Proc. Natl Acad. Sci. USA
107, 22687–22692 (2010).
Yiu, A. P., Rashid, A. J. & Josselyn, S. A.
Increasing CREB function in the CA1 region of dorsal hippocampus rescues the spatial memory deficits in a mouse model of Alzheimer's disease. Neuropsychopharmacology
36, 2169–2186 (2011).
Santos, S. F., Pierrot, N. & Octave, J. N.
Network excitability dysfunction in Alzheimer's disease: insights from in vitro and in vivo models. Rev. Neurosci.
21, 153–171 (2010).
Disterhoft, J. F. & Oh, M. M.
Alterations in intrinsic neuronal excitability during normal aging. Aging Cell
6, 327–336 (2007).
Stan, A. D. & Lewis, D. A.
Altered cortical GABA neurotransmission in schizophrenia: insights into novel therapeutic strategies. Curr. Pharm. Biotechnol.
13, 1557–1562 (2012).
Nader, K. & Hardt, O.
A single standard for memory: the case for reconsolidation. Nature Rev. Neurosci.
10, 224–234 (2009).
Frankland, P. W. & Bontempi, B.
The organization of recent and remote memories. Nature Rev. Neurosci.
6, 119–130 (2005).