Repetitive motor learning induces coordinated formation of clustered dendritic spines in vivo.
TLDR
These findings suggest that clustering of new synapses along dendrites is induced by repetitive activation of the cortical circuitry during learning, providing a structural basis for spatial coding of motor memory in the mammalian brain.Abstract:
Many lines of evidence suggest that memory in the mammalian brain is stored with distinct spatiotemporal patterns. Despite recent progresses in identifying neuronal populations involved in memory coding, the synapse-level mechanism is still poorly understood. Computational models and electrophysiological data have shown that functional clustering of synapses along dendritic branches leads to nonlinear summation of synaptic inputs and greatly expands the computing power of a neural network. However, whether neighbouring synapses are involved in encoding similar memory and how task-specific cortical networks develop during learning remain elusive. Using transcranial two-photon microscopy, we followed apical dendrites of layer 5 pyramidal neurons in the motor cortex while mice practised novel forelimb skills. Here we show that a third of new dendritic spines (postsynaptic structures of most excitatory synapses) formed during the acquisition phase of learning emerge in clusters, and that most such clusters are neighbouring spine pairs. These clustered new spines are more likely to persist throughout prolonged learning sessions, and even long after training stops, than non-clustered counterparts. Moreover, formation of new spine clusters requires repetition of the same motor task, and the emergence of succedent new spine(s) accompanies the strengthening of the first new spine in the cluster. We also show that under control conditions new spines appear to avoid existing stable spines, rather than being uniformly added along dendrites. However, succedent new spines in clusters overcome such a spatial constraint and form in close vicinity to neighbouring stable spines. Our findings suggest that clustering of new synapses along dendrites is induced by repetitive activation of the cortical circuitry during learning, providing a structural basis for spatial coding of motor memory in the mammalian brain.read more
Citations
More filters
Journal ArticleDOI
Labelling and optical erasure of synaptic memory traces in the motor cortex
Akiko Hayashi-Takagi,Sho Yagishita,Mayumi Nakamura,Fukutoshi Shirai,Yi I. Wu,Amanda L. Loshbaugh,Brian Kuhlman,Klaus M. Hahn,Haruo Kasai +8 more
TL;DR: A novel synaptic optoprobe is developed that can label recently potentiated spines specifically, and induce the selective shrinkage of AS-PaRac1-containing spines, demonstrating that a newly acquired motor skill depends on the formation of a task-specific dense synaptic ensemble.
Journal ArticleDOI
Dendritic Spines: The Locus of Structural and Functional Plasticity
Carlo Sala,Menahem Segal +1 more
TL;DR: Issues with respect to spine formation and plasticity are addressed and the complexity of molecular pathways involved in regulation of spine structure and function is highlighted, which contributes to the understanding of central synaptic interactions in health and disease.
Journal ArticleDOI
Structural plasticity upon learning: regulation and functions
TL;DR: The new findings suggest that a mechanistic understanding of learning and memory processes will require monitoring ensembles of synapses in situ and the development of synaptic network models that combine changes in synaptic function and connectivity.
Journal ArticleDOI
Dendritic integration: 60 years of progress
Gregory J Stuart,Nelson Spruston +1 more
TL;DR: Six decades of progress are reviewed, which collectively highlights the complex ways that single neurons integrate their inputs, emphasizing the critical role of dendrites in information processing in the brain.
Journal ArticleDOI
Neural Manifolds for the Control of Movement.
TL;DR: A model for neural control of movement in which the time-dependent activation of these neural modes is the generator of motor behavior is discussed, which may lead to a better understanding of how the brain controls movement.
References
More filters
Journal ArticleDOI
Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP.
Guoping Feng,Rebecca H. Mellor,Michael L. Bernstein,Cynthia Keller-Peck,Quyen T. Nguyen,Mia Wallace,Jeanne M. Nerbonne,Jeff W. Lichtman,Joshua R. Sanes +8 more
TL;DR: Each of 25 independently generated transgenic lines expressed XFP in a unique pattern, even though all incorporated identical regulatory elements (from the thyl gene), for example, all retinal ganglion cells or many cortical neurons were XFP positive in some lines, whereas only a few ganglions or only layer 5 cortical pyramids were labeled in others.
Neurotechnique Imaging Neuronal Subsets in Transgenic Mice Expressing Multiple Spectral Variants of GFP
Guoping Feng,Rebecca H. Mellor,Michael L. Bernstein,Cynthia Keller-Peck,Quyen T. Nguyen,Mia Wallace,Jeanne M. Nerbonne,Jeff W. Lichtman,Joshua R. Sanes +8 more
Journal ArticleDOI
Experience-dependent structural synaptic plasticity in the mammalian brain.
Anthony Holtmaat,Karel Svoboda +1 more
TL;DR: Recent evidence for structural forms of synaptic plasticity in the mammalian cortex involves cell type-specific structural plasticity: some boutons and dendritic spines appear and disappear, accompanied by synapse formation and elimination, respectively.
Journal ArticleDOI
Long-term dendritic spine stability in the adult cortex
TL;DR: It is shown that filopodia-like dendritic protrusions, extending and retracting over hours, are abundant in young animals but virtually absent from the adult, providing a potential structural basis for long-term information storage.
Journal ArticleDOI
Rapid formation and selective stabilization of synapses for enduring motor memories
Tonghui Xu,Xinzhu Yu,Andrew J. Perlik,Willie F. Tobin,Jonathan A. Zweig,Kelly A. Tennant,Theresa A. Jones,Yi Zuo +7 more
TL;DR: It is shown that synaptic connections in the living mouse brain rapidly respond to motor-skill learning and permanently rewire, and that stabilized neuronal connections are the foundation of durable motor memory.
Related Papers (5)
Stably maintained dendritic spines are associated with lifelong memories
Guang Yang,Feng Pan,Wen-Biao Gan +2 more