Tag and capture: how salient experiences target and rescue nearby events in memory

Abstract

The long-term fate of a memory is not exclusively determined by the events occurring at the moment of encoding. Research at the cellular, circuit, and behavioral levels is beginning to reveal how neurochemical activations in the moments surrounding an event can retroactively and proactively rescue weak memory for seemingly mundane experiences. We review emerging evidence showing enhancement of weakly formed memories encoded minutes to hours before or after a related motivationally relevant experience. We discuss proposed neurobiological mechanisms for strengthening weak memories formed in temporal proximity to a strong event, and how this knowledge could be leveraged to improve memory for information that is prone to forgetting.

Keywords: conditioning; emotion; episodic; memory; novelty; retroactive.

Figure 1.. Tag-and-capture at the cellular and behavioral level

(A) Simplified schematic of synaptic tag-and-capture at the cellular level. Weak stimulation at a synaptic pathway (early-LTP) sets a tag insufficient to produce a long-term memory (late-LTP). Strong stimulation in a different synaptic pathway, from the same neural ensemble, synthesizes release of plasticity-related proteins (PRPs). These PRPs are now accessible and can be “captured” by the weakly stimulated synaptic pathway. (B) The behavioral tagging hypothesis proposes that strong experiences serve as potentiating events that bolster memory for weakly learned experiences encoded before or after the strong event. (C) Commonly used laboratory tasks to test behavioral tagging mostly utilize hippocampus-dependent learning, including tests of episodic memory in humans. (D) A number of boundary conditions and pharmacological manipulations interfere with proactive and retroactive enhancements of memory generated via novelty, establishing the behavioral tagging hypothesis as a testable phenomenon.

Figure 2.. Proposed neural mechanisms by which salient events retroactively augment weak memory.

(Left panel) Weak encoding of unique information (Category A and Category B) sets transient learning tags in separate neural ensembles. (Middle panel) Building on the Glutamate Amplifies Noradrenergic Effects (GANE) model, release of norepinephrine (NE) may exert different effects on regions transmitting high (Category B) and low (Category A) priority inputs by engaging the facilitating and inhibitory effects of different adrenoreceptors, respectively. NE release may suppress weak sensory inputs to the Category A ensemble and weaken synaptic plasticity by engaging the inhibitory effects of high affinity alpha2- and alpha1-adrenoreceptors, respectively. Coincident release of NE with strong sensory inputs to the Category B ensemble triggers a positive glutamate-NE feedback loop, or ‘hotspot’, that upregulates local excitation and NE concentration. This self-strengthening feedback loop generate high enough NE levels to engage low affinity beta-adrenoreceptors (green boxes) that enhance neural activity and synaptic plasticity in the Category B ensemble. Building on synaptic tag-and-capture, beta-adrenoreceptor activation triggers the production of the plasticity-related proteins (PRP’s) to stabilize recently established learning tags. The opposing effects of NE on strong and weak patterns of brain activity thereby amplifies the effects of priority in memory consolidation. A salient event also triggers the dopaminergic system to synthesize release of PRP’s to enhance consolidation in those same high priority pathways. (Right panel) Memory selection processes may continue to occur “offline” after the strong experience. According to this adaptive systems consolidation perspective, strong experiences bias post-encoding hippocampal communication towards sensory cortical regions representing a now-significant category of information. This shift in hippocampal processes privileges selective consolidation of distantly encountered information that overlaps with the significant event. Together, these online and offline processes help to explain how the brain adaptively prioritizes and preserves mundane memories that acquire significance in the future.