Learning-Related Synaptic Reconfiguration in Hippocampal Networks: Memory Storage or Waveguide Tuning?

Eduardo Mercado III; Eduardo Mercado III

doi:10.3934/Neuroscience.2015.1.28

AIMS Neuroscience

2015, Volume 2, Issue 1: 28-34. doi: 10.3934/Neuroscience.2015.1.28

Previous Article Next Article

Commentary Special Issues

Learning-Related Synaptic Reconfiguration in Hippocampal Networks: Memory Storage or Waveguide Tuning?

Eduardo Mercado III ^,

Department of Psychology, University at Buffalo, Buffalo, NY 14260, USA

Received: 17 February 2015 Accepted: 27 February 2015 Published: 02 March 2015

A fundamental assumption of current hypotheses regarding hippocampal involvement in memory formation is that changes in synaptic connections between hippocampal neurons serve to encode information about recent events. An alternative possibility is that synaptic changes are “ruts” left by dynamic traveling waves involved in memory processes rather than a mechanism for storing memories of events. Specifically, traveling waves of activity in corticohippocampal circuits may sometimes modify those circuits as they propagate through them, thereby changing the paths and qualities of future wave patterns.
- basal forebrain,
- cholinergic modulation,
- conditioning,
- cortical waves,
- neural plasticity
Citation: Eduardo Mercado III. Learning-Related Synaptic Reconfiguration in Hippocampal Networks: Memory Storage or Waveguide Tuning?[J]. AIMS Neuroscience, 2015, 2(1): 28-34. doi: 10.3934/Neuroscience.2015.1.28

Related Papers:

Abstract

A fundamental assumption of current hypotheses regarding hippocampal involvement in memory formation is that changes in synaptic connections between hippocampal neurons serve to encode information about recent events. An alternative possibility is that synaptic changes are “ruts” left by dynamic traveling waves involved in memory processes rather than a mechanism for storing memories of events. Specifically, traveling waves of activity in corticohippocampal circuits may sometimes modify those circuits as they propagate through them, thereby changing the paths and qualities of future wave patterns.

References

[1]	Lomo T (1966) Frequency potentiation of excitatory synaptic activity in the dentate area of the hippocampal formation. Acta Physiol Scand 68: 128.
[2]	Shors TJ, Matzel LD (1997) Long-term potentiation: What's learning got to do with it? Behav Brain Sci 20: 597-614;
[3]	Baudry M, Bi X, Gall C, et al. (2011) The biochemistry of memory: The 26 year journey of a 'new and specific hypothesis'. Neurobiol Learn Mem 95: 125-133. doi: 10.1016/j.nlm.2010.11.015
[4]	Buzsaki G (2010) Neural syntax: Cell assemblies, synapsembles, and readers. Neuron 68:362-385. doi: 10.1016/j.neuron.2010.09.023
[5]	Squire LR, Wixted JT (2011) The cognitive neuroscience of human memory since H.M. Annu Rev Neurosci 34: 259-288. doi: 10.1146/annurev-neuro-061010-113720
[6]	Rissman J, Wagner AD (2012) Distributed representations in memory: Insights from functional brain imaging. Annu Rev Psychol 63: 101-128. doi: 10.1146/annurev-psych-120710-100344
[7]	Rudy JW (2014) The neurobiology of learning and memory. Sunderland, MA: Sinauer Associates.
[8]	Mitsushima D (2015) Contextual learning requires functional diversity at excitatory and inhibitory synapses onto CA1 pyramidal neurons. AIMS Neurosci 2: 7-17. doi: 10.3934/Neuroscience.2015.1.7
[9]	Mitsushima D, Sano A, Takahashi T (2013) A cholinergic trigger drives learning-induced plasticity at hippocampal synapses. Nat Commun 4: 2760.
[10]	Takeuchi T, Duszkiewicz AJ, Morris RG (2014) The synaptic plasticity and memory hypothesis: Encoding, storage and persistence. Philos Trans R Soc Lond B Biol Sci 369: 20130288.
[11]	Whitlock JR, Heynen AJ, Shuler MG, et al. (2006) Learning induces long-term potentiation in the hippocampus. Science 313: 1093-1097. doi: 10.1126/science.1128134
[12]	Bakin JS, Weinberger NM (1996) Induction of a physiological memory in the cerebral cortex by stimulation of the nucleus basalis. Proc Natl Acad Sci U S A 93: 11219-11224. doi: 10.1073/pnas.93.20.11219
[13]	Mercado E, III, Bao S, Orduna I, et al. (2001) Basal forebrain stimulation changes cortical sensitivities to complex sound. Neuroreport 12: 2283-2287. doi: 10.1097/00001756-200107200-00047
[14]	Froemke RC, Carcea I, Barker AJ, et al. (2013) Long-term modification of cortical synapses improves sensory perception. Nat Neurosci 16: 79-88.
[15]	Froemke RC, Merzenich MM, Schreiner CE (2007) A synaptic memory trace for cortical receptive field plasticity. Nature 450: 425-429. doi: 10.1038/nature06289
[16]	Marrosu F, Portas C, Mascia MS, et al. (1995) Microdialysis measurement of cortical and hippocampal acetylcholine release during sleep-wake cycle in freely moving cats. Brain Res 671:329-332. doi: 10.1016/0006-8993(94)01399-3
[17]	Newman EL, Gupta K, Climer JR, et al. (2012) Cholinergic modulation of cognitive processing: Insights drawn from computational models. Front Behav Neurosci 6: 24.
[18]	Rokers B, Mercado E, III, Allen MT, et al. (2002) A connectionist model of septohippocampal dynamics during conditioning: Closing the loop. Behav Neurosci 116: 48-62. doi: 10.1037/0735-7044.116.1.48
[19]	Manseau F, Goutagny R, Danik M, et al. (2008) The hippocamposeptal pathway generates rhythmic firing of GABAergic neurons in the medial septum and diagonal bands: An investigation using a complete septohippocampal preparation in vitro. J Neurosci 28: 4096-4107. doi: 10.1523/JNEUROSCI.0247-08.2008
[20]	Zhang H, Lin SC, Nicolelis MA (2010) Spatiotemporal coupling between hippocampal acetylcholine release and theta oscillations in vivo. J Neurosci 30: 13431-13440. doi: 10.1523/JNEUROSCI.1144-10.2010
[21]	Vandecasteele M, Varga V, Berenyi A, et al. (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. doi: 10.1073/pnas.1411233111
[22]	Ajemian R, D'Ausilio A, Moorman H, et al. (2013) A theory for how sensorimotor skills are learned and retained in noisy and nonstationary neural circuits. Proc Natl Acad Sci U S A 110: E5078-5087. doi: 10.1073/pnas.1320116110
[23]	Routtenberg A (2013) Lifetime memories from persistently supple synapses. Hippocampus 23:202-206. doi: 10.1002/hipo.22088
[24]	Routtenberg A (2008) Long-lasting memory from evanescent networks. Eur J Pharmacol 585:60-63. doi: 10.1016/j.ejphar.2008.02.047
[25]	Routtenberg A (2008) The substrate for long-lasting memory: If not protein synthesis, then what? Neurobiol Learn Mem 89: 225-233. doi: 10.1016/j.nlm.2007.10.012
[26]	Richards BA, Frankland PW (2013) The conjunctive trace. Hippocampus 23: 207-212. doi: 10.1002/hipo.22089
[27]	Chen N, Sugihara H, Sharma J, et al. (2012) Nucleus basalis-enabled stimulus-specific plasticity in the visual cortex is mediated by astrocytes. Proc Natl Acad Sci U S A 109: E2832-2841. doi: 10.1073/pnas.1206557109
[28]	McKenzie IA, Ohayon D, Li H, et al. (2014) Motor skill learning requires active central myelination. Science 346: 318-322. doi: 10.1126/science.1254960
[29]	Patel J, Fujisawa S, Berenyi A, et al. (2012) Traveling theta waves along the entire septotemporal axis of the hippocampus. Neuron 75: 410-417. doi: 10.1016/j.neuron.2012.07.015
[30]	Lubenov EV, Siapas AG (2009) Hippocampal theta oscillations are travelling waves. Nature 459:534-539. doi: 10.1038/nature08010
[31]	Benchenane K, Peyrache A, Khamassi M, et al. (2010) Coherent theta oscillations and reorganization of spike timing in the hippocampal- prefrontal network upon learning. Neuron 66:921-936. doi: 10.1016/j.neuron.2010.05.013
[32]	Siapas AG, Lubenov EV, Wilson MA (2005) Prefrontal phase locking to hippocampal theta oscillations. Neuron 46: 141-151. doi: 10.1016/j.neuron.2005.02.028
[33]	Sirota A, Montgomery S, Fujisawa S, et al. (2008) Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron 60: 683-697. doi: 10.1016/j.neuron.2008.09.014
[34]	Buzsaki G (2005) Theta rhythm of navigation: Link between path integration and landmark navigation, episodic and semantic memory. Hippocampus 15: 827-840. doi: 10.1002/hipo.20113
[35]	Landfield PW, McGaugh JL, Tusa RJ (1972) Theta rhythm: A temporal correlate of memory storage processes in the rat. Science 175: 87-89. doi: 10.1126/science.175.4017.87
[36]	Miller R (1989) Cortico-hippocampal interplay: Self-organizing phase-locked loops for indexing memory. Psychobiol 17: 115-128.
[37]	Palmer JH, Gong P (2014) Associative learning of classical conditioning as an emergent property of spatially extended spiking neural circuits with synaptic plasticity. Front Comput Neurosci 8: 79.
[38]	Battaglia FP, Benchenane K, Sirota A, et al. (2011) The hippocampus: Hub of brain network communication for memory. Trends Cogn Sci 15: 310-318.
[39]	Lansdell B, Ford K, Kutz JN (2014) A reaction-diffusion model of cholinergic retinal waves.PLoS Comput Biol 10: e1003953. doi: 10.1371/journal.pcbi.1003953
[40]	Wester JC, Contreras D (2012) Columnar interactions determine horizontal propagation of recurrent network activity in neocortex. J Neurosci 32: 5454-5471. doi: 10.1523/JNEUROSCI.5006-11.2012
[41]	Pavlov IP (1927) Conditioned reflexes. London: Oxford University Press.
[42]	Griffen TC, Wang L, Fontanini A, et al. (2012) Developmental regulation of spatio-temporal patterns of cortical circuit activation. Front Cell Neurosci 6: 65.
[43]	Wang L, Fontanini A, Maffei A (2011) Visual experience modulates spatio-temporal dynamics of circuit activation. Front Cell Neurosci 5: 12.
[44]	Blankenship AG, Feller MB (2010) Mechanisms underlying spontaneous patterned activity in developing neural circuits. Nat Rev Neurosci 11: 18-29. doi: 10.1038/nrn2759
[45]	Palagina G, Eysel UT, Jancke D (2009) Strengthening of lateral activation in adult rat visual cortex after retinal lesions captured with voltage-sensitive dye imaging in vivo. Proc Natl Acad Sci U S A 106: 8743-8747. doi: 10.1073/pnas.0900068106
[46]	Ponulak F, Hopfield JJ (2013) Rapid, parallel path planning by propagating wavefronts of spiking neural activity. Front Comput Neurosci 7: 98.
[47]	Mercado E, III (2014) Relating cortical wave dynamics to learning and remembering. AIMS Neurosci 1: 185-209. doi: 10.3934/Neuroscience.2014.3.185
[48]	Heitmann S, Gong P, Breakspear M (2012) A computational role for bistability and traveling waves in motor cortex. Front Comput Neurosci 6: 67.
[49]	Gong P, van Leeuwen C (2009) Distributed dynamical computation in neural circuits with propagating coherent activity patterns. PLoS Comput Biol 5: e1000611. doi: 10.1371/journal.pcbi.1000611

Reader Comments

Your name:*

Email:*
© 2015 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)