Randomly Fluctuating Neural Connections May Implement a Consolidation Mechanism That Explains Classic Memory Laws

Overview

Journal Sci Rep

Specialty Science

Date 2022 Aug 4

PMID 35927567

Authors

Jaap M J Murre

Affiliations

Soon will be listed here.

Abstract

How can we reconcile the massive fluctuations in neural connections with a stable long-term memory? Two-photon microscopy studies have revealed that large portions of neural connections (spines, synapses) are unexpectedly active, changing unpredictably over time. This appears to invalidate the main assumption underlying the majority of memory models in cognitive neuroscience, which rely on stable connections that retain information over time. Here, we show that such random fluctuations may in fact implement a type of memory consolidation mechanism with a stable very long-term memory that offers novel explanations for several classic memory 'laws', namely Jost's Law (1897: superiority of spaced learning) and Ribot's Law (1881: loss of recent memories in retrograde amnesia), for which a common neural basis has been postulated but not established, as well as other general 'laws' of learning and forgetting. We show how these phenomena emerge naturally from massively fluctuating neural connections.

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References

van der Zee E . Synapses, spines and kinases in mammalian learning and memory, and the impact of aging. Neurosci Biobehav Rev. 2014; 50:77-85. DOI: 10.1016/j.neubiorev.2014.06.012. View

Berry K, Nedivi E . Spine Dynamics: Are They All the Same?. Neuron. 2017; 96(1):43-55. PMC: 5661952. DOI: 10.1016/j.neuron.2017.08.008. View

Alvarez V, Sabatini B . Anatomical and physiological plasticity of dendritic spines. Annu Rev Neurosci. 2007; 30:79-97. DOI: 10.1146/annurev.neuro.30.051606.094222. View

Yasumatsu N, Matsuzaki M, Miyazaki T, Noguchi J, Kasai H . Principles of long-term dynamics of dendritic spines. J Neurosci. 2008; 28(50):13592-608. PMC: 2706274. DOI: 10.1523/JNEUROSCI.0603-08.2008. View

Beatty W, Salmon D, Butters N, Heindel W, Granholm E . Retrograde amnesia in patients with Alzheimer's disease or Huntington's disease. Neurobiol Aging. 1988; 9(2):181-6. DOI: 10.1016/s0197-4580(88)80048-4. View

Rosenblatt F . The perceptron: a probabilistic model for information storage and organization in the brain. Psychol Rev. 1958; 65(6):386-408. DOI: 10.1037/h0042519. View

McClelland J, Rogers T . The parallel distributed processing approach to semantic cognition. Nat Rev Neurosci. 2003; 4(4):310-22. DOI: 10.1038/nrn1076. View

Segal M . Dendritic spines and long-term plasticity. Nat Rev Neurosci. 2005; 6(4):277-84. DOI: 10.1038/nrn1649. View

Kopelman M . Remote and autobiographical memory, temporal context memory and frontal atrophy in Korsakoff and Alzheimer patients. Neuropsychologia. 1989; 27(4):437-60. DOI: 10.1016/0028-3932(89)90050-x. View

10.

Fauth M, Worgotter F, Tetzlaff C . Formation and Maintenance of Robust Long-Term Information Storage in the Presence of Synaptic Turnover. PLoS Comput Biol. 2015; 11(12):e1004684. PMC: 4699846. DOI: 10.1371/journal.pcbi.1004684. View

11.

Holtmaat A, De Paola V, Wilbrecht L, Knott G . Imaging of experience-dependent structural plasticity in the mouse neocortex in vivo. Behav Brain Res. 2008; 192(1):20-5. DOI: 10.1016/j.bbr.2008.04.005. View

12.

Wixted J . On Common Ground: Jost's (1897) law of forgetting and Ribot's (1881) law of retrograde amnesia. Psychol Rev. 2004; 111(4):864-79. DOI: 10.1037/0033-295X.111.4.864. View

13.

Frank A, Huang S, Zhou M, Gdalyahu A, Kastellakis G, Silva T . Hotspots of dendritic spine turnover facilitate clustered spine addition and learning and memory. Nat Commun. 2018; 9(1):422. PMC: 5789055. DOI: 10.1038/s41467-017-02751-2. View

14.

Antal M, Fukazawa Y, Eordogh M, Muszil D, Molnar E, Itakura M . Numbers, densities, and colocalization of AMPA- and NMDA-type glutamate receptors at individual synapses in the superficial spinal dorsal horn of rats. J Neurosci. 2008; 28(39):9692-701. PMC: 3844880. DOI: 10.1523/JNEUROSCI.1551-08.2008. View

15.

Benna M, Fusi S . Computational principles of synaptic memory consolidation. Nat Neurosci. 2016; 19(12):1697-1706. DOI: 10.1038/nn.4401. View

16.

McClelland J, McNaughton B, OReilly R . 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. 1995; 102(3):419-457. DOI: 10.1037/0033-295X.102.3.419. View

17.

Stefanacci L, Buffalo E, Schmolck H, Squire L . Profound amnesia after damage to the medial temporal lobe: A neuroanatomical and neuropsychological profile of patient E. P. J Neurosci. 2000; 20(18):7024-36. PMC: 6772843. View

18.

Sikstrom S . Forgetting curves: implications for connectionist models. Cogn Psychol. 2002; 45(1):95-152. DOI: 10.1016/s0010-0285(02)00012-9. View

19.

Murre J, Chessa A . Power laws from individual differences in learning and forgetting: mathematical analyses. Psychon Bull Rev. 2011; 18(3):592-7. PMC: 3098361. DOI: 10.3758/s13423-011-0076-y. View

20.

Matsuzaki M . Factors critical for the plasticity of dendritic spines and memory storage. Neurosci Res. 2006; 57(1):1-9. DOI: 10.1016/j.neures.2006.09.017. View