Synaptic Ensemble Underlying the Selection and Consolidation of Neuronal Circuits during Learning

Abstract

Memories are crucial to the cognitive essence of who we are as human beings. Accumulating evidence has suggested that memories are stored as a subset of neurons that probably fire together in the same ensemble. Such formation of cell ensembles must meet contradictory requirements of being plastic and responsive during learning, but also stable in order to maintain the memory. Although synaptic potentiation is presumed to be the cellular substrate for this process, the link between the two remains correlational. With the application of the latest optogenetic tools, it has been possible to collect direct evidence of the contributions of synaptic potentiation in the formation and consolidation of cell ensemble in a learning task specific manner. In this review, we summarize the current view of the causative role of synaptic plasticity as the cellular mechanism underlying the encoding of memory and recalling of learned memories. In particular, we will be focusing on the latest optoprobe developed for the visualization of such “synaptic ensembles.” We further discuss how a new synaptic ensemble could contribute to the formation of cell ensembles during learning and memory. With the development and application of novel research tools in the future, studies on synaptic ensembles will pioneer new discoveries, eventually leading to a comprehensive understanding of how the brain works.

Mild metabolic stress is sufficient to disturb the formation of pyramidal cell ensembles during gamma oscillations

“…1) Selective coupling, implying that neurons recruited in an ensemble have privileged connections. This is crucial for having temporal matrices were individual neurons know when to fire action potentials in synchrony with other members of the same ensemble (Hoshiba et al, 2017).…”

“…An ensemble of neurons can be assembled rapidly during the exploration of a new environment encoding spatial information. For this to be accomplished, networks should be adaptable and plastic for the unlimited number of new environments that can be explored (Hoshiba et al, 2017;Neves et al, 2008;Zarnadze et al, 2016). 5) Background suppression.…”

Intrinsic excitability mechanisms of neuronal ensemble formation

“…The function of brain is anchored on the activity of groups of connected neurons, forming microcircuits (Schüz and Braitenberg, 2001;Shepherd, 2004). These groups of coactive neurons, or ensembles (also known as assemblies or attractors), exhibit synchronous or correlated activity (Lorente De Nó, 1938;Hebb, 1949;Hopfield, 1982;Abeles, 1991;Cossart et al, 2003;Buzsáki, 2010;Miller et al, 2014;Yuste, 2015;Carrillo-Reid et al, 2016Marshel et al, 2019), and appear critical for brain function (Hoshiba et al, 2017) and memory formation (Hebb, 1949). In the cerebral cortex, these states may arise from patterns of multineural activity that persist spontaneously after an initial stimulus, generating recurrent activity (reverberations) (Lorente de Nó, 1933;Churchland and Sejnowski, 1992).…”

“…One mechanism that fulfills Hebb's rule is Long-Term Synaptic Potentiation (LTP), originally defined as a long-lasting increase in synaptic efficacy after a high frequency burst electrical stimulation (Bliss and Gardner-Medwin, 1973). Accordingly, changes in synaptic weights produces preferential connectivity that controls the flow of activity within and between neuronal ensembles (Hoshiba et al, 2017). Since its initial discovery (Bliss and Gardner-Medwin, 1973), LTP has been widely established as the cellular correlate for memory and learning.…”

Vocal motor experiences consolidate the vocal motor circuitry and accelerate future vocal skill development

“…The finding that the re-acquisition of song performance progresses considerably faster than the initial acquisition, and leads to the production of highly similar song patterns suggests that singing skills are retained during intermittent silent periods. Motor learning and memory are generally considered to rely on the maturation and consolidation of the synaptic connections within the neural circuitry that drives the behavior in question (36)(37)(38). To investigate changes in synaptic connectivity during vocal motor development, we quantified the number of neuronal dendritic spines in the forebrain motor nucleus HVC before, during, and after the acquisition of vocal motor skills ( Fig.…”