Labelling and optical erasure of synaptic memory traces in the motor cortex

Hayashi‐Takagi, Akiko; Yagishita, Sho; Nakamura, Mayumi; Shirai, Fukutoshi; Wu, Yi; Loshbaugh, Amanda L.; Kuhlman, Brian; Hahn, Klaus M.; Kasai, Hideaki

doi:10.1038/nature15257

Cited by 581 publications

(533 citation statements)

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“…Alternatively, our results may instead represent a direct interaction between MIo and SIo. The dense anatomical connections between MIo and SIo provide a substrate for coherent firing of neurons that may underlie the formation of neuronal assemblies (2,38,39). Thus, the increased proportion of coherent neurons may represent the new coupling of a motor output to specific sensory inputs as learning unfolds.…”

Section: Discussionmentioning

confidence: 99%

Primary motor and sensory cortical areas communicate via spatiotemporally coordinated networks at multiple frequencies

Arce-McShane

Ross

Takahashi

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Skilled movements rely on sensory information to shape optimal motor responses, for which the sensory and motor cortical areas are critical. How these areas interact to mediate sensorimotor integration is largely unknown. Here, we measure intercortical coherence between the orofacial motor (MIo) and somatosensory (SIo) areas of cortex as monkeys learn to generate tongue-protrusive force. We report that coherence between MIo and SIo is reciprocal and that neuroplastic changes in coherence gradually emerge over a few days. These functional networks of coherent spiking and local field potentials exhibit frequency-specific spatiotemporal properties. During force generation, theta coherence (2-6 Hz) is prominent and exhibited by numerous paired signals; before or after force generation, coherence is evident in alpha (6-13 Hz), beta (15-30 Hz), and gamma (30-50 Hz) bands, but the functional networks are smaller and weaker. Unlike coherence in the higher frequency bands, the distribution of the phase at peak theta coherence is bimodal with peaks near 0°and ±180°, suggesting that communication between somatosensory and motor areas is coordinated temporally by the phase of theta coherence. Time-sensitive sensorimotor integration and plasticity may rely on coherence of local and large-scale functional networks for cortical processes to operate at multiple temporal and spatial scales.S ynchrony between cortical areas has been implicated in neuronal communication and plasticity (1-4). Sensorimotor integration and formation of motor memories during learning are examples wherein effective communication between sensory and motor areas of the cerebral cortex is critical. However, very few studies have investigated coherence between the somatosensory and motor pathways in primates (5-7). These past studies have been confined to upper limb tasks, and none of them looked at changes in coherence during learning. Here, we investigated the synchronous activity between the orofacial primary motor (MIo) and somatosensory (SIo) cortical areas that play important roles in the control of orofacial behaviors (8-10). Sensorimotor control of oral behaviors is complex, involving the integration of afferent information for moving the tongue and facial muscles. Anatomical connections between MIo and SIo are dense and both areas have bilateral orofacial representations and project to brainstem cranial nerve motor nuclei containing the motoneurons projecting to jaw, facial, and tongue muscles (11,12). These connections provide a substrate for interareal communication between MIo and SIo for the control and learning of orofacial behaviors. To investigate cortico-cortical interactions between these areas, we measured coherence of spiking and local field potentials (LFPs) recorded simultaneously from MIo and SIo of the left hemisphere as monkeys learned a simple and controlled tongue protrusion task. Several studies using this behavioral paradigm have reported neuroplasticity and modulation of neuronal activity related to tongue protrusion separatel...

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Section: Discussionmentioning

confidence: 99%

Primary motor and sensory cortical areas communicate via spatiotemporally coordinated networks at multiple frequencies

Arce-McShane

Ross

Takahashi

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…Hebbian mechanisms have correlates in synaptic structural plasticity, in which LTP is correlated with the formation of new spines [71,72], and LTD is associated with the loss of pre-existing spines [73]. The in vivo upregulation of spine dynamics has been observed following sensory deprivation in somatosensory cortex [74 -77], olfactory cortex [78,79], auditory cortex [80] and visual cortex [74,77,81 -83], and following learning in motor cortex [84][85][86] where the memory of the learned motor task depends on the newly formed synapses [87].…”

Section: Similarities Across Brain Regions In Vivomentioning

confidence: 99%

Integrating Hebbian and homeostatic plasticity: the current state of the field and future research directions

Keck

Toyoizumi

Chen

et al. 2017

Phil. Trans. R. Soc. B

194

192

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We summarize here the results presented and subsequent discussion from the meeting on Integrating Hebbian and Homeostatic Plasticity at the Royal Society in April 2016. We first outline the major themes and results presented at the meeting. We next provide a synopsis of the outstanding questions that emerged from the discussion at the end of the meeting and finally suggest potential directions of research that we believe are most promising to develop an understanding of how these two forms of plasticity interact to facilitate functional changes in the brain.This article is part of the themed issue 'Integrating Hebbian and homeostatic plasticity'.

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“…NMDAR heterotetramers are composed of obligatory GluN1 subunits as well as a variable configuration of GluN2A-D and GluN3A-B subunits (Cull-Candy et al, 2001;Paoletti et al, 2013). Differences in NMDAR composition throughout development regulate synapse stability and plasticity.…”

Section: Introductionmentioning

confidence: 99%

“…Integrin ␣3␤1 adhesion receptor signaling through the Abl2/Arg nonreceptor tyrosine kinase (Arg) is critical for dendrite arbor and synapse stability. Neurons lacking integrin ␣3␤1 or Arg develop normally through postnatal day 21 (P21), but then exhibit widespread dendrite, dendritic spine, and synapse loss by P42 (Sfakianos et al, 2007;Gourley et al, 2012;Kerrisk et al, 2013). Integrin-Arg signaling stabilizes dendrite arbors by activating the Rho GTPase inhibitor p190RhoGAP to attenuate RhoA signaling (Sfakianos et al, 2007;Gourley et al, 2012;Kerrisk et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Disruption of Coordinated Presynaptic and Postsynaptic Maturation Underlies the Defects in Hippocampal Synapse Stability and Plasticity in Abl2/Arg-Deficient Mice

Xiao

Levy²,

Rosenberg³

et al. 2016

J. Neurosci.

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Immature glutamatergic synapses in cultured neurons contain high-release probability (P r ) presynaptic sites coupled to postsynaptic sites bearing GluN2B-containing NMDA receptors (NMDARs), which mature into low-P r , GluN2B-deficient synapses. Whether this coordinated maturation of high-P r , GluN2B ϩ synapses to low-P r , GluN2B-deficient synapses actually occurs in vivo, and if so, what factors regulate it and what role it might play in long-term synapse function and plasticity are unknown. We report that loss of the integrinregulated Abl2/Arg kinase in vivo yields a subpopulation of "immature" high-P r , GluN2B ϩ hippocampal synapses that are maintained throughout late postnatal development and early adulthood. These high-P r , GluN2B ϩ synapses are evident in arg Ϫ/Ϫ animals as early as postnatal day 21 (P21), a time that precedes any observable defects in synapse or dendritic spine number or structure in arg Ϫ/Ϫ mice. Using focal glutamate uncaging at individual synapses, we find only a subpopulation of arg Ϫ/Ϫ spines exhibits increased GluN2B-mediated responses at P21. As arg Ϫ/Ϫ mice age, these synapses increase in proportion, and their associated spines enlarge. These changes coincide with an overall loss of spines and synapses in the Arg-deficient mice. We also demonstrate that, although LTP and LTD are normal in P21 arg Ϫ/Ϫ slices, both forms of plasticity are significantly altered by P42. These data demonstrate that the integrin-regulated Arg kinase coordinates the maturation of presynaptic and postsynaptic compartments in a subset of hippocampal synapses in vivo, and this coordination is critical for NMDAR-dependent long-term synaptic stability and plasticity.

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Labelling and optical erasure of synaptic memory traces in the motor cortex

Cited by 581 publications

References 50 publications

Primary motor and sensory cortical areas communicate via spatiotemporally coordinated networks at multiple frequencies

Primary motor and sensory cortical areas communicate via spatiotemporally coordinated networks at multiple frequencies

Integrating Hebbian and homeostatic plasticity: the current state of the field and future research directions

Disruption of Coordinated Presynaptic and Postsynaptic Maturation Underlies the Defects in Hippocampal Synapse Stability and Plasticity in Abl2/Arg-Deficient Mice

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