Cellular tagging as a neural network mechanism for behavioural tagging

Abstract

Behavioural tagging is the transformation of a short-term memory, induced by a weak experience, into a long-term memory (LTM) due to the temporal association with a novel experience. The mechanism by which neuronal ensembles, each carrying a memory engram of one of the experiences, interact to achieve behavioural tagging is unknown. Here we show that retrieval of a LTM formed by behavioural tagging of a weak experience depends on the degree of overlap with the neuronal ensemble corresponding to a novel experience. The numbers of neurons activated by weak training in a novel object recognition (NOR) task and by a novel context exploration (NCE) task, denoted as overlapping neurons, increases in the hippocampal CA1 when behavioural tagging is successfully achieved. Optical silencing of an NCE-related ensemble suppresses NOR–LTM retrieval. Thus, a population of cells recruited by NOR is tagged and then preferentially incorporated into the memory trace for NCE to achieve behavioural tagging.

Effects of post-training novelty exposure on contextual fear memory: An attempt to translate behavioral tagging to humans

“…In humans, behavioral tagging might be more pronounced in tasks that involve explicit memory processes, or spatial navigation, rather than implicit fear conditioning. Future work should consider whether behavioral tagging can rescue weak spatial object learning in humans, which would still be in keeping with several rodent investigations of behavioral tagging (Ballarini et al 2009; Wang et al 2010; Nomoto et al 2016; Moncada 2017).…”

“…In rodents, this includes tasks for spatial learning (Wang et al 2010), object recognition (Ballarini et al 2009), inhibitory avoidance (Moncada et al 2011), and contextual fear conditioning and extinction (Ballarini et al 2009; de Carvalho Myskiw et al 2013; de Carvalho Myskiw et al 2014; Menezes et al 2015). In the behavioral tagging model, weak learning sets the conditions for a long-term memory; but in line with the synaptic tag-and-capture model (Frey and Morris 1997), long-term memory formation is dependent upon stronger synaptic potentiation within overlapping neural ensemble during a critical time window around the time of training (Nomoto et al 2016). Novelty exploration provides the conditions for strong synaptic potentiation by triggering upregulation of plasticity related proteins in the hippocampus (Straube et al 2003) necessary to stabilize local learning tags set by the weak learning experience.…”

“…The goal of the present study was to develop a protocol to translate behavioral tagging research from rodents (e.g., Moncada and Viola 2007; Ballarini et al 2009; Wang et al 2010; de Carvalho Myskiw et al 2013; Nomoto et al 2016; Gros and Wang 2018) to humans. To date, there is some indirect evidence in support of a behavioral tagging mechanism in human episodic memory research.…”

On the research of time past: the hunt for the substrate of memory

“…If these neurons are directly reactivated (i.e., with light), the memory, or more specifically the behavioral readout of the target memory, can be elicited . If the cells are inhibited, the natural cue‐induced recall of the target memory is impaired . Control experiments have shown that activation and inhibition of these cell ensembles affects the targeted memory specifically, not other similar but nonlabelled memories .…”

“…56,59 If the cells are inhibited, the natural cue-induced recall of the target memory is impaired. 60,61,[66][67][68] Control experiments have shown that activation and inhibition of these cell ensembles affects the targeted memory specifically, not other similar but nonlabelled memories. 56,[58][59][60] If the labelled neural ensembles are destroyed, so too is the memory.…”