Behavioral tagging and the penumbra of learning

In noisy, dynamic environments, organisms must distinguish genuine change (e.g., the movement of prey) from noise (e.g., the rustling of leaves). Expectations should be updated only when the organism believes genuine change has occurred. Although individual variables can be highly unreliable, organisms can take advantage of the fact that changes tend to be correlated (e.g., movement of prey will tend to produce changes in both visual and olfactory modalities). Thus, observing a change in one variable provides information about the rate of change for other variables. We call this the penumbra of learning. At the neural level, the penumbra of learning may offer an explanation for why strong plasticity in one synapse can rescue weak plasticity at another (synaptic tagging and capture). At the behavioral level, it has been observed that weak learning of one task can be rescued by novelty exposure before or after the learning task. Here, using a simple number prediction task, we provide direct behavioral support for the penumbra of learning in humans, and show that it can be accounted for by a normative computational theory of learning.

[1]  M. Merhav,et al.  Facilitation of taste memory acquisition by experiencing previous novel taste is protein-synthesis dependent. , 2008, Learning & memory.

[2]  Petros G. Voulgaris,et al.  On optimal ℓ∞ to ℓ∞ filtering , 1995, Autom..

[3]  G. Turrigiano The Self-Tuning Neuron: Synaptic Scaling of Excitatory Synapses , 2008, Cell.

[4]  D. Madison,et al.  Locally distributed synaptic potentiation in the hippocampus. , 1994, Science.

[5]  Joshua I. Gold,et al.  Bayesian Online Learning of the Hazard Rate in Change-Point Problems , 2010, Neural Computation.

[6]  Angela J. Yu,et al.  Uncertainty, Neuromodulation, and Attention , 2005, Neuron.

[7]  Robert C. Wilson,et al.  Rational regulation of learning dynamics by pupil–linked arousal systems , 2012, Nature Neuroscience.

[8]  U. Frey,et al.  Synaptic tagging and long-term potentiation , 1997, Nature.

[9]  S. Sajikumar,et al.  Late-associativity, synaptic tagging, and the role of dopamine during LTP and LTD , 2004, Neurobiology of Learning and Memory.

[10]  Jonathan D. Cohen,et al.  An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. , 2005, Annual review of neuroscience.

[11]  U. Frey,et al.  Weak before strong: dissociating synaptic tagging and plasticity-factor accounts of late-LTP , 1998, Neuropharmacology.

[12]  R. Morris,et al.  Relevance of synaptic tagging and capture to the persistence of long-term potentiation and everyday spatial memory , 2010, Proceedings of the National Academy of Sciences.

[13]  S. Gershman On the Blessing of Abstraction , 2017, Quarterly journal of experimental psychology.

[14]  Samuel J Gershman,et al.  The penumbra of learning: A statistical theory of synaptic tagging and capture , 2014, Network.

[15]  D. Moncada,et al.  Induction of Long-Term Memory by Exposure to Novelty Requires Protein Synthesis: Evidence for a Behavioral Tagging , 2007, The Journal of Neuroscience.

[16]  F. Ballarini,et al.  Identification of transmitter systems and learning tag molecules involved in behavioral tagging during memory formation , 2011, Proceedings of the National Academy of Sciences.

[17]  K. Duncan,et al.  Memory’s Penumbra: Episodic Memory Decisions Induce Lingering Mnemonic Biases , 2012, Science.

[18]  R. Morris,et al.  Making memories last: the synaptic tagging and capture hypothesis , 2010, Nature Reviews Neuroscience.

[19]  Timothy E. J. Behrens,et al.  Learning the value of information in an uncertain world , 2007, Nature Neuroscience.

[20]  J. Pearce,et al.  A model for Pavlovian learning: variations in the effectiveness of conditioned but not of unconditioned stimuli. , 1980, Psychological review.

[21]  Guillem R. Esber,et al.  Surprise! Neural correlates of Pearce–Hall and Rescorla–Wagner coexist within the brain , 2012, The European journal of neuroscience.