Sleep spindles coordinate corticostriatal reactivations during the emergence of automaticity

2020 ◽  
Author(s):  
S. M. Lemke ◽  
D. S. Ramanathan ◽  
D. Darevsky ◽  
D. Egert ◽  
J. D. Berke ◽  
...  
Keyword(s):  
Primary Motor Cortex ◽  
Activity Patterns ◽  
Behavioral Flexibility ◽  
Sleep Spindles ◽  
Behavioral Consistency ◽  
Natural Activity ◽  
Trigger Activity ◽  
Corticostriatal Plasticity ◽  
Repeated Training ◽  
Activity Dependent

Plasticity within the corticostriatal network is known to regulate the balance between behavioral flexibility and automaticity. Repeated training of an action has been shown to bias behavior towards automaticity, suggesting that training may trigger activity-dependent corticostriatal plasticity. However, surprisingly little is known about the natural activity patterns that may drive plasticity or when they occur during long-term training. Here we chronically monitored neural activity from primary motor cortex (M1) and the dorsolateral striatum (DLS) during both training and offline periods, i.e., time away from training including sleep, throughout the development of an automatic reaching action. We first show that blocking striatal NMDA receptors during offline periods prevents the emergence of behavioral consistency, a hallmark of automaticity. We then show that, throughout the development of an automatic reaching action, corticostriatal functional connectivity increases during offline periods. Such increases track the emergence of consistent behavior and predictable cross-area neural dynamics. We then identify sleep spindles during non-REM sleep (NREM) as uniquely poised to mediate corticostriatal plasticity during offline periods. We show that sleep spindles are periods of maximal corticostriatal transmission within offline periods, that sleep spindles in post-training NREM reactivate neurons across areas, and that sleep-spindle modulation in post-training NREM is linked to observable changes in spiking relationships between individual pairs of M1 and DLS neurons. Our results indicate that offline periods, in general, and sleep spindles, specifically, play an important role in regulating behavioral flexibility through corticostriatal network plasticity.

scholarly journals Coupling between motor cortex and striatum increases during sleep over long-term skill learning

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Stefan M Lemke ◽  
Dhakshin S Ramanathan ◽  
David Darevksy ◽  
Daniel Egert ◽  
Joshua D Berke ◽  
...  
Keyword(s):  
Nrem Sleep ◽  
Skill Learning ◽  
Neural Dynamics ◽  
Sleep Spindles ◽  
Behavioral Variability ◽  
Slow Oscillations ◽  
Corticostriatal Plasticity ◽  
Repeated Training ◽  
Time Away

The strength of cortical connectivity to the striatum influences the balance between behavioral variability and stability. Learning to consistently produce a skilled action requires plasticity in corticostriatal connectivity associated with repeated training of the action. However, it remains unknown whether such corticostriatal plasticity occurs during training itself or 'offline' during time away from training, such as sleep. Here, we monitor the corticostriatal network throughout long-term skill learning in rats and find that non-REM (NREM) sleep is a relevant period for corticostriatal plasticity. We first show that the offline activation of striatal NMDA receptors is required for skill learning. We then show that corticostriatal functional connectivity increases offline, coupled to emerging consistent skilled movements and coupled cross-area neural dynamics. We then identify NREM sleep spindles as uniquely poised to mediate corticostriatal plasticity, through interactions with slow oscillations. Our results provide evidence that sleep shapes cross-area coupling required for skill learning.

scholarly journals Differential Effects of Open- and Closed-Loop Intracortical Microstimulation on Firing Patterns of Neurons in Distant Cortical Areas

2019 ◽  
Vol 30 (5) ◽  
pp. 2879-2896 ◽  
Author(s):  
Alberto Averna ◽  
Valentina Pasquale ◽  
Maxwell D Murphy ◽  
Maria Piera Rogantin ◽  
Gustaf M Van Acker ◽  
...  
Keyword(s):  
Closed Loop ◽  
Activity Patterns ◽  
Brain Lesion ◽  
Progressive Increase ◽  
Intracortical Microstimulation ◽  
Behavioral Recovery ◽  
Firing Patterns ◽  
Electrical Microstimulation ◽  
Spike Patterns ◽  
Activity Dependent

Abstract Intracortical microstimulation can be used successfully to modulate neuronal activity. Activity-dependent stimulation (ADS), in which action potentials recorded extracellularly from a single neuron are used to trigger stimulation at another cortical location (closed-loop), is an effective treatment for behavioral recovery after brain lesion, but the related neurophysiological changes are still not clear. Here, we investigated the ability of ADS and random stimulation (RS) to alter firing patterns of distant cortical locations. We recorded 591 neuronal units from 23 Long-Evan healthy anesthetized rats. Stimulation was delivered to either forelimb or barrel field somatosensory cortex, using either RS or ADS triggered from spikes recorded in the rostral forelimb area (RFA). Both RS and ADS stimulation protocols rapidly altered spike firing within RFA compared with no stimulation. We observed increase in firing rates and change of spike patterns. ADS was more effective than RS in increasing evoked spikes during the stimulation periods, by producing a reliable, progressive increase in stimulus-related activity over time and an increased coupling of the trigger channel with the network. These results are critical for understanding the efficacy of closed-loop electrical microstimulation protocols in altering activity patterns in interconnected brain networks, thus modulating cortical state and functional connectivity.

scholarly journals Coupling an aVLSI Neuromorphic Vision Chip to a Neurotrophic Model of Synaptic Plasticity: The Development of Topography

2002 ◽  
Vol 14 (10) ◽  
pp. 2353-2370 ◽  
Author(s):  
Terry Elliott ◽  
Jörg Kramer
Keyword(s):  
Synaptic Plasticity ◽  
Neuronal Development ◽  
Ganglion Cells ◽  
Activity Patterns ◽  
Retinal Ganglion ◽  
Biologically Inspired ◽  
Silicon Neurons ◽  
Retina Chip ◽  
Developing System ◽  
Activity Dependent

We couple a previously studied, biologically inspired neurotrophic model of activity-dependent competitive synaptic plasticity and neuronal development to a neuromorphic retina chip. Using this system, we examine the development and refinement of a topographic mapping between an array of afferent neurons (the retinal ganglion cells) and an array of target neurons. We find that the plasticity model can indeed drive topographic refinement in the presence of afferent activity patterns generated by a real-world device. We examine the resilience of the developing system to the presence of high levels of noise by adjusting the spontaneous firing rate of the silicon neurons.

scholarly journals GluA4 subunit of AMPA receptors mediates the early synaptic response to altered network activity in the developing hippocampus

2016 ◽  
Vol 115 (6) ◽  
pp. 2989-2996 ◽  
Author(s):  
J. Huupponen ◽  
T. Atanasova ◽  
T. Taira ◽  
S. E. Lauri
Keyword(s):  
Ampa Receptors ◽  
Pyramidal Neurons ◽  
Activity Patterns ◽  
Critical Role ◽  
Long Term Potentiation ◽  
Postnatal Period ◽  
Homeostatic Plasticity ◽  
Network Activity ◽  
Hippocampal Pyramidal Neurons ◽  
Activity Dependent

Development of the neuronal circuitry involves both Hebbian and homeostatic plasticity mechanisms that orchestrate activity-dependent refinement of the synaptic connectivity. AMPA receptor subunit GluA4 is expressed in hippocampal pyramidal neurons during early postnatal period and is critical for neonatal long-term potentiation; however, its role in homeostatic plasticity is unknown. Here we show that GluA4-dependent plasticity mechanisms allow immature synapses to promptly respond to alterations in network activity. In the neonatal CA3, the threshold for homeostatic plasticity is low, and a 15-h activity blockage with tetrodotoxin triggers homeostatic upregulation of glutamatergic transmission. On the other hand, attenuation of the correlated high-frequency bursting in the CA3-CA1 circuitry leads to weakening of AMPA transmission in CA1, thus reflecting a critical role for Hebbian synapse induction in the developing CA3-CA1. Both of these developmentally restricted forms of plasticity were absent in GluA4 −/− mice. These data suggest that GluA4 enables efficient homeostatic upscaling and responsiveness to temporal activity patterns during the critical period of activity-dependent refinement of the circuitry.

scholarly journals Activity-dependent inhibitory synapse remodeling through gephyrin phosphorylation

2014 ◽  
Vol 112 (1) ◽  
pp. E65-E72 ◽  
Author(s):  
Carmen E. Flores ◽  
Irina Nikonenko ◽  
Pablo Mendez ◽  
Jean-Marc Fritschy ◽  
Shiva K. Tyagarajan ◽  
...  
Keyword(s):  
Activity Patterns ◽  
Phosphorylation Site ◽  
Morphological Plasticity ◽  
Long Term Potentiation ◽  
Inhibitory Synapse ◽  
Inhibitory Synapses ◽  
Synapse Plasticity ◽  
Inhibitory Plasticity ◽  
And Function ◽  
Activity Dependent

Maintaining a proper balance between excitation and inhibition is essential for the functioning of neuronal networks. However, little is known about the mechanisms through which excitatory activity can affect inhibitory synapse plasticity. Here we used tagged gephyrin, one of the main scaffolding proteins of the postsynaptic density at GABAergic synapses, to monitor the activity-dependent adaptation of perisomatic inhibitory synapses over prolonged periods of time in hippocampal slice cultures. We find that learning-related activity patterns known to induce N-methyl-d-aspartate (NMDA) receptor-dependent long-term potentiation and transient optogenetic activation of single neurons induce within hours a robust increase in the formation and size of gephyrin-tagged clusters at inhibitory synapses identified by correlated confocal electron microscopy. This inhibitory morphological plasticity was associated with an increase in spontaneous inhibitory activity but did not require activation of GABAA receptors. Importantly, this activity-dependent inhibitory plasticity was prevented by pharmacological blockade of Ca2+/calmodulin-dependent protein kinase II (CaMKII), it was associated with an increased phosphorylation of gephyrin on a site targeted by CaMKII, and could be prevented or mimicked by gephyrin phospho-mutants for this site. These results reveal a homeostatic mechanism through which activity regulates the dynamics and function of perisomatic inhibitory synapses, and they identify a CaMKII-dependent phosphorylation site on gephyrin as critically important for this process.

Activity-dependent changes in intrinsic excitability of human spinal motoneurones produced by natural activity

2012 ◽  
Vol 108 (9) ◽  
pp. 2473-2480 ◽  
Author(s):  
Alessandro Rossi ◽  
Simone Rossi ◽  
Federica Ginanneschi
Keyword(s):  
Action Potential ◽  
Compound Muscle Action Potential ◽  
Intrinsic Excitability ◽  
Dependent Manner ◽  
Natural Activity ◽  
Muscle Action Potential ◽  
Abductor Digiti Minimi ◽  
F Wave ◽  
Spinal Motoneurones ◽  
Activity Dependent

The current study was designed to evaluate activity-dependent changes intrinsic to the spinal motoneurones (MNs) associated with sustained contractions. The excitability of spinal MNs (reflected by the antidromically evoked F-wave) innervating the abductor digiti minimi muscle (ADM) was measured in 12 healthy subjects following maximum voluntary contractions (MVCs) of ADM lasting 5 s, 15 s, 30 s, and 60 s. Upon cessation of the contractions, F-waves showed a depression, which increased in depth and duration with increasing duration of contraction. Following a 5-s contraction, there was a 20% decrease, which waned in 2 min, whereas a 60-s contraction produced a 40% decrease and waned in over 15 min. The changes in excitability of peripheral motor axons produced by the MVCs were measured by recording an ADM compound muscle action potential (CMAP) of ∼50% of maximum to a constant ulnar nerve electrical stimulation. On cessation of the contractions, there was a prominent decrease in size of the CMAP: following a 5-s MVC, it produced a 10% decrease in the size of the test CMAP, which recovered in 2 min, whereas following a 60-s MVC, it produced a 30% decrease, which recovered in over 15 min. Statistical analysis (correntropy) showed a high-order mutual dependence between F-wave and CMAP, and both were significantly dependent on MVC duration. Because of the parallel excitability changes in peripheral axons and spinal MNs, our interpretation is that intrinsic excitability of the axon initial segment (i.e., where the action potential is generated) and peripheral axon segments changed in a similar, activity-dependent manner.

scholarly journals Motor planning brings human primary somatosensory cortex into action-specific preparatory states

eLife ◽  
2022 ◽  
Vol 11 ◽  
Author(s):  
Giacomo Ariani ◽  
J Andrew Pruszynski ◽  
Jörn Diedrichsen
Keyword(s):  
Somatosensory Cortex ◽  
Motor Neurons ◽  
Primary Motor Cortex ◽  
Specific Activity ◽  
Activity Patterns ◽  
Critical Role ◽  
Motor Planning ◽  
Movement Control ◽  
Movement Planning ◽  
Primary Somatosensory Cortex

Motor planning plays a critical role in producing fast and accurate movement. Yet, the neural processes that occur in human primary motor and somatosensory cortex during planning, and how they relate to those during movement execution, remain poorly understood. Here we used 7T functional magnetic resonance imaging (fMRI) and a delayed movement paradigm to study single finger movement planning and execution. The inclusion of no-go trials and variable delays allowed us to separate what are typically overlapping planning and execution brain responses. Although our univariate results show widespread deactivation during finger planning, multivariate pattern analysis revealed finger-specific activity patterns in contralateral primary somatosensory cortex (S1), which predicted the planned finger action. Surprisingly, these activity patterns were as informative as those found in contralateral primary motor cortex (M1). Control analyses ruled out the possibility that the detected information was an artifact of subthreshold movements during the preparatory delay. Furthermore, we observed that finger-specific activity patterns during planning were highly correlated to those during execution. These findings reveal that motor planning activates the specific S1 and M1 circuits that are engaged during the execution of a finger press, while activity in both regions is overall suppressed. We propose that preparatory states in S1 may improve movement control through changes in sensory processing or via direct influence of spinal motor neurons.

scholarly journals Intracellular calcium stores mediate a synapse-specific form of metaplasticity at hippocampal dendritic spines

2018 ◽  
Author(s):  
Gaurang Mahajan ◽  
Suhita Nadkarni
Keyword(s):  
Dendritic Spines ◽  
Activity Patterns ◽  
Long Term Potentiation ◽  
Multiple Time Scales ◽  
Calcium Stores ◽  
Multiple Time ◽  
Additional Layer ◽  
Term Potentiation ◽  
Activity Dependent

ABSTRACTLong-term plasticity mediated by NMDA receptors supports input-specific, Hebbian forms of learning at excitatory CA3-CA1 connections in the hippocampus. An additional layer of stabilizing mechanisms that act globally as well as locally over multiple time scales may be in place to ensure that plasticity occurs in a constrained manner. Here, we investigate the potential role of calcium (Ca2+) stores associated with the endoplasmic reticulum (ER) in the local regulation of plasticity dynamics at individual CA1 synapses. Our study is spurred by (1) the curious observation that ER is sparsely distributed in dendritic spines, but over-represented in large spines that are likely to have undergone activity-dependent strengthening, and (2) evidence suggesting that ER motility within synapses can be rapid, and accompany activity-regulated spine remodeling. Based on a physiologically realistic computational model for ER-bearing CA1 spines, we characterize the contribution of IP3-sensitive Ca2+ stores to spine Ca2+ dynamics during activity patterns mimicking the induction of long-term potentiation (LTP) and depression (LTD). Our results suggest graded modulation of the NMDA receptor-dependent plasticity profile by ER, which selectively enhances LTD induction. We propose that spine ER can locally tune Ca2+-based plasticity on an as-needed basis, providing a braking mechanism to mitigate runaway strengthening at potentiated synapses. Our model suggests that the presence of ER in the CA1 spine may promote re-use of synapses with saturated strengths.

scholarly journals Homeostatic activity-dependent tuning of recurrent networks for robust propagation of activity

2015 ◽  
Author(s):  
Julijana Gjorgjieva ◽  
Jan Felix Evers ◽  
Stephen Eglen
Keyword(s):  
Spontaneous Activity ◽  
Activity Patterns ◽  
Network Connectivity ◽  
Recurrent Network ◽  
Recurrent Networks ◽  
Synaptic Growth ◽  
Network Output ◽  
Homeostatic Model ◽  
Weak Connectivity ◽  
Activity Dependent

Developing neuronal networks display spontaneous rhythmic bursts of action potentials that are necessary for circuit organization and tuning. While spontaneous activity has been shown to instruct map formation in sensory circuits, it is unknown whether it plays a role in the organization of motor networks that produce rhythmic output. Using computational modeling we investigate how recurrent networks of excitatory and inhibitory neuronal populations assemble to produce robust patterns of unidirectional and precisely-timed propagating activity during organism locomotion. One example is provided by the motor network in Drosophila larvae, which generates propagating peristaltic waves of muscle contractions during crawling. We examine two activity-dependent models which tune weak network connectivity based on spontaneous activity patterns: a Hebbian model, where coincident activity in neighboring populations strengthens connections between them; and a homeostatic model, where connections are homeostatically regulated to maintain a constant level of excitatory activity based on spontaneous input. The homeostatic model tunes network connectivity to generate robust activity patterns with the appropriate timing relationships between neighboring populations. These timing relationships can be modulated by the properties of spontaneous activity suggesting its instructive role for generating functional variability in network output. In contrast, the Hebbian model fails to produce the tight timing relationships between neighboring populations required for unidirectional activity propagation, even when additional assumptions are imposed to constrain synaptic growth. These results argue that homeostatic mechanisms are more likely than Hebbian mechanisms to tune weak connectivity based on local activity patterns in a recurrent network for rhythm generation and propagation.

scholarly journals Rotating waves during human sleep spindles organize global patterns of activity that repeat precisely through the night

eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Lyle Muller ◽  
Giovanni Piantoni ◽  
Dominik Koller ◽  
Sydney S Cash ◽  
Eric Halgren ◽  
...  
Keyword(s):  
Large Scale ◽  
Activity Patterns ◽  
Neural Mechanism ◽  
Sleep Spindles ◽  
Sleep Spindle ◽  
Spike Time ◽  
Temporal Precision ◽  
Global Patterns ◽  
Spike Time Dependent Plasticity ◽  
Large Scale Networks

During sleep, the thalamus generates a characteristic pattern of transient, 11-15 Hz sleep spindle oscillations, which synchronize the cortex through large-scale thalamocortical loops. Spindles have been increasingly demonstrated to be critical for sleep-dependent consolidation of memory, but the specific neural mechanism for this process remains unclear. We show here that cortical spindles are spatiotemporally organized into circular wave-like patterns, organizing neuronal activity over tens of milliseconds, within the timescale for storing memories in large-scale networks across the cortex via spike-time dependent plasticity. These circular patterns repeat over hours of sleep with millisecond temporal precision, allowing reinforcement of the activity patterns through hundreds of reverberations. These results provide a novel mechanistic account for how global sleep oscillations and synaptic plasticity could strengthen networks distributed across the cortex to store coherent and integrated memories.

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