Micro-rewiring As a Substrate for Learning

Overview

Journal Trends Neurosci

Specialty Neurology

Date 2008 Sep 27

PMID 18817991

Citations 18

Authors

William M DeBello

Affiliations

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Abstract

How does the brain encode life experiences? Recent results derived from vital imaging, computational modeling, cellular physiology and systems neuroscience have pointed to local changes in synaptic connectivity as a powerful substrate, here termed micro-rewiring. To examine this hypothesis, I first review findings on micro-structural dynamics with focus on the extension and retraction of dendritic spines. Although these observations demonstrate a biological mechanism, they do not inform us of the specific changes in circuit configuration that might occur during learning. Here, computational models have made testable predictions for both the neuronal and circuit levels. Integrative approaches in the mammalian neocortex and the barn owl auditory localization pathway provide some of the first direct evidence in support of these 'synaptic-clustering' mechanisms. The implications of these data and the challenges for future research are discussed.

Citing Articles

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Emergence of Stable Synaptic Clusters on Dendrites Through Synaptic Rewiring.

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References

Shoham S, OConnor D, Sarkisov D, Wang S . Rapid neurotransmitter uncaging in spatially defined patterns. Nat Methods. 2005; 2(11):837-43. DOI: 10.1038/nmeth793. View

Kelleher K, Hajdik V, Colbert C, Josic K . Learning by structural remodeling in a class of single cell models. J Comput Neurosci. 2008; 25(2):282-95. DOI: 10.1007/s10827-008-0078-6. View

Lee W, Huang H, Feng G, Sanes J, Brown E, So P . Dynamic remodeling of dendritic arbors in GABAergic interneurons of adult visual cortex. PLoS Biol. 2005; 4(2):e29. PMC: 1318477. DOI: 10.1371/journal.pbio.0040029. View

Gasparini S, Magee J . State-dependent dendritic computation in hippocampal CA1 pyramidal neurons. J Neurosci. 2006; 26(7):2088-100. PMC: 6674927. DOI: 10.1523/JNEUROSCI.4428-05.2006. View

de Paola V, Holtmaat A, Knott G, Song S, Wilbrecht L, Caroni P . Cell type-specific structural plasticity of axonal branches and boutons in the adult neocortex. Neuron. 2006; 49(6):861-75. DOI: 10.1016/j.neuron.2006.02.017. View

Stettler D, Yamahachi H, Li W, Denk W, Gilbert C . Axons and synaptic boutons are highly dynamic in adult visual cortex. Neuron. 2006; 49(6):877-87. DOI: 10.1016/j.neuron.2006.02.018. View

Losonczy A, Magee J . Integrative properties of radial oblique dendrites in hippocampal CA1 pyramidal neurons. Neuron. 2006; 50(2):291-307. DOI: 10.1016/j.neuron.2006.03.016. View

Govindarajan A, Kelleher R, Tonegawa S . A clustered plasticity model of long-term memory engrams. Nat Rev Neurosci. 2006; 7(7):575-83. DOI: 10.1038/nrn1937. View

Holtmaat A, Wilbrecht L, Knott G, Welker E, Svoboda K . Experience-dependent and cell-type-specific spine growth in the neocortex. Nature. 2006; 441(7096):979-83. DOI: 10.1038/nature04783. View

10.

Sjostrom P, Hausser M . A cooperative switch determines the sign of synaptic plasticity in distal dendrites of neocortical pyramidal neurons. Neuron. 2006; 51(2):227-38. PMC: 7616902. DOI: 10.1016/j.neuron.2006.06.017. View

11.

Knott G, Holtmaat A, Wilbrecht L, Welker E, Svoboda K . Spine growth precedes synapse formation in the adult neocortex in vivo. Nat Neurosci. 2006; 9(9):1117-24. DOI: 10.1038/nn1747. View

12.

Le Be J, Markram H . Spontaneous and evoked synaptic rewiring in the neonatal neocortex. Proc Natl Acad Sci U S A. 2006; 103(35):13214-9. PMC: 1559779. DOI: 10.1073/pnas.0604691103. View

13.

Letzkus J, Kampa B, Stuart G . Learning rules for spike timing-dependent plasticity depend on dendritic synapse location. J Neurosci. 2006; 26(41):10420-9. PMC: 6674691. DOI: 10.1523/JNEUROSCI.2650-06.2006. View

14.

Araya R, Eisenthal K, Yuste R . Dendritic spines linearize the summation of excitatory potentials. Proc Natl Acad Sci U S A. 2006; 103(49):18799-804. PMC: 1693742. DOI: 10.1073/pnas.0609225103. View

15.

Walter J, Khodakhah K . The linear computational algorithm of cerebellar Purkinje cells. J Neurosci. 2006; 26(50):12861-72. PMC: 6674952. DOI: 10.1523/JNEUROSCI.4507-05.2006. View

16.

Kimberley McAllister A . Dynamic aspects of CNS synapse formation. Annu Rev Neurosci. 2007; 30:425-50. PMC: 3251656. DOI: 10.1146/annurev.neuro.29.051605.112830. View

17.

Micheva K, Smith S . Array tomography: a new tool for imaging the molecular architecture and ultrastructure of neural circuits. Neuron. 2007; 55(1):25-36. PMC: 2080672. DOI: 10.1016/j.neuron.2007.06.014. View

18.

Lendvai B, Stern E, Chen B, Svoboda K . Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo. Nature. 2000; 404(6780):876-81. DOI: 10.1038/35009107. View

19.

Poirazi P, Mel B . Impact of active dendrites and structural plasticity on the memory capacity of neural tissue. Neuron. 2001; 29(3):779-96. DOI: 10.1016/s0896-6273(01)00252-5. View

20.

Williams S, Stuart G . Dependence of EPSP efficacy on synapse location in neocortical pyramidal neurons. Science. 2002; 295(5561):1907-10. DOI: 10.1126/science.1067903. View