Motor learning selectively strengthens cortical and striatal synapses of motor engram neurons

Hwang, Fuu-Jiun; Roth, Richard H.; Wu, Yuwei; Sun, Yue; Kwon, Destany K; Liu, Yu; Ding, Jun

doi:10.1016/j.neuron.2022.06.006

Cited by 55 publications

(53 citation statements)

References 63 publications

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“…In other words, coordination of firing between pre-synaptic neurons reduces the number of pre-synaptic spike trains needed to produce LTP. The mean distance between spines in the experimentally observed clusters on SPN dendrites was ~10

m [ 92 ], which is consistent with our observation that smaller clusters are more likely to exhibit LTP.…”

Section: Discussionsupporting

confidence: 90%

“…Complementing these in vitro findings, correlated activity in spatially clustered spines has been observed in vivo in pyramidal neurons [ 9 , 89 , 90 , 91 ], and in vivo calcium transients in neighboring spines of the same dendritic branch correlate with structural potentiation of spines in motor cortical neurons [ 80 ]. In the striatum, a recent study showed that SPN spines that are innervated by motor cortex pyramidal neurons involved in learning are clustered on dendrites [ 92 ]. Building on these findings, our work predicts that neighboring synaptic interactions can influence the direction and magnitude of corticostriatal synaptic plasticity in vivo, with high neighboring activity producing a larger magnitude of both LTP and LTD, and smaller clusters tending to produce LTP.…”

Section: Discussionmentioning

confidence: 99%

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Synaptic Plasticity Is Predicted by Spatiotemporal Firing Rate Patterns and Robust to In Vivo-like Variability

Dorman

Blackwell

2022

Biomolecules

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Synaptic plasticity, the experience-induced change in connections between neurons, underlies learning and memory in the brain. Most of our understanding of synaptic plasticity derives from in vitro experiments with precisely repeated stimulus patterns; however, neurons exhibit significant variability in vivo during repeated experiences. Further, the spatial pattern of synaptic inputs to the dendritic tree influences synaptic plasticity, yet is not considered in most synaptic plasticity rules. Here, we investigate how spatiotemporal synaptic input patterns produce plasticity with in vivo-like conditions using a data-driven computational model with a plasticity rule based on calcium dynamics. Using in vivo spike train recordings as inputs to different size clusters of spines, we show that plasticity is strongly robust to trial-to-trial variability of spike timing. In addition, we derive general synaptic plasticity rules describing how spatiotemporal patterns of synaptic inputs control the magnitude and direction of plasticity. Synapses that strongly potentiated have greater firing rates and calcium concentration later in the trial, whereas strongly depressing synapses have hiring firing rates early in the trial. The neighboring synaptic activity influences the direction and magnitude of synaptic plasticity, with small clusters of spines producing the greatest increase in synaptic strength. Together, our results reveal that calcium dynamics can unify diverse plasticity rules and reveal how spatiotemporal firing rate patterns control synaptic plasticity.

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m [ 92 ], which is consistent with our observation that smaller clusters are more likely to exhibit LTP.…”

Section: Discussionsupporting

confidence: 90%

Section: Discussionmentioning

confidence: 99%

Synaptic Plasticity Is Predicted by Spatiotemporal Firing Rate Patterns and Robust to In Vivo-like Variability

Dorman

Blackwell

2022

Biomolecules

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“…Specifically, we used a multivoxel local correlation pattern (MVLC) analysis, similar to a previously used approach for evaluating memory reactivation in the human brain 16,28 , to determine whether reactivation may depend on transient changes in Glu and GABA following learning. Cortico-striatal interactions are critically implicated in the consolidation of motor memories 7,12,29 ; We therefore also examined the relationship between the dynamics of Glu and GABA in M1 shortly after learning, and the inter-regional communication of M1 and the putamen as quantified using resting state BOLD data. Lastly, since motor skill learning has been shown to induce plastic changes in M1, we investigated whether changes in Glu and GABA following learning may be related to structural and functional plasticity in M1, as expressed by overnight changes in the GM volume and functional connectivity of this region.…”

Section: Introductionmentioning

confidence: 99%

“…Furthermore, motor memory consolidation has been shown to be associated with structural and functional plasticity in M1 on multiple levels 1 . Microstructural changes, such as dendritic spines remodelling, have been demonstrated in animals following motor learning 7 , while macroscopic changes in grey matter (GM) volume were observed in humans 8 . In addition, changes in the functional communication between M1 and related brain regions have been shown following the acquisition of new skills 9–12 , highlighting the importance of early post-learning functional modifications to the learning outcomes 9 .…”

Section: Introductionmentioning

confidence: 99%

Early excitatory and inhibitory modifications in the motor cortex following skill learning support motor memory consolidation and cortical plasticity overnight

Eisenstein

Furman‐Haran

Tal

2022

Preprint

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The learning of new motor skills constitutes an inseparable part of our lives. Motor consolidation refers to the offline processing of motor memories following the acquisition of new motor skills. The animal literature suggests that the primary motor cortex (M1) plays a key role in motor memory consolidation, and structural and functional plasticity in M1 following motor consolidation have been demonstrated. However, the mechanisms supporting motor memory consolidation and plasticity in the human M1 are not well understood. Initial human neuroimaging studies show that the initial stages of motor learning in humans are accompanied by short-term temporal dynamics of the brain main excitatory and inhibitory neurotransmitters, Glutamate (Glu) and GABA, in M1, but it remains unclear how these relate to the question of motor memory consolidation. Here, we show that early Glu and GABA modifications in M1 following motor skill learning may play vital roles in supporting motor memory consolidation and neural plasticity that take place over longer time scales. Using a multimodal magnetic resonance approach implemented on ultra-high field 7T scanner in healthy young adults (n=36), we found increased Glu and decreased GABA in M1 during the initial offline period following learning to support consolidation-related local and inter-regional functions of M1, such as motor memory reactivation and increased functional connectivity with the striatum. These neurochemical changes also correlated with overnight structural and functional plasticity expressed as increased M1 grey matter volume and functional connectivity, while Glu modifications also correlated with adaptive behavior, as reflected by improvements in skill performance. Our results provide intriguing microscale mechanistic evidence to the potential distinctive roles of Glu and GABA in promoting motor memory consolidation and plasticity in the human M1. They also highlight a role for early neurochemical modifications to memory consolidation and plasticity in the human brain and may hold important clinical implications in rehabilitative settings such as in stroke and brain injury.

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“…In a new study, researchers observed synaptic changes when mice performed motor tasks to learn more about memory engram (cognitive information imprinted on physical substance) in the brain [1]. When mice learned to use their pawn in a tricky maneuver for getting food, specific neurons in the primary motor cortex (M1) were activated.…”

mentioning

confidence: 99%

The brain works hard to learn physical skills

AISDL¹

2022

Preprint

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Motor learning selectively strengthens cortical and striatal synapses of motor engram neurons

Cited by 55 publications

References 63 publications

Synaptic Plasticity Is Predicted by Spatiotemporal Firing Rate Patterns and Robust to In Vivo-like Variability

Synaptic Plasticity Is Predicted by Spatiotemporal Firing Rate Patterns and Robust to In Vivo-like Variability

Early excitatory and inhibitory modifications in the motor cortex following skill learning support motor memory consolidation and cortical plasticity overnight

The brain works hard to learn physical skills

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