Total recall: episodic memory retrieval, choice, and memory confidence in the rat

Episodic memory enables recollection of past experiences to guide future behavior. Humans know which memories to trust (high confidence) and which to doubt (low confidence). How memory retrieval, memory confidence, and memory-guided decisions are related, however, is not understood. Additionally, whether animals can assess confidence in episodic memories to guide behavior is unknown. We developed a spatial episodic memory task in which rats were incentivized to gamble their time: betting more following a correct choice yielded greater reward. Rat behavior reflected memory confidence, with higher temporal bets following correct choices. We applied modern machine learning to identify a memory decision variable, and built a generative model of memories evolving over time that accurately predicted both choices and confidence reports. Our results reveal in rats an ability thought to exist exclusively in primates, and introduce a unified model of memory dynamics, retrieval, choice, and confidence.

[1]  Adam Kepecs,et al.  Behavior- and Modality-General Representation of Confidence in Orbitofrontal Cortex , 2020, Cell.

[2]  A. Soltani,et al.  Contributions of anterior cingulate cortex and basolateral amygdala to decision confidence and learning under uncertainty , 2019, Nature Communications.

[3]  S. M. Etesami,et al.  An embedding technique to determine ττ backgrounds in proton-proton collision data , 2019 .

[4]  M. Buckley,et al.  Mnemonic Introspection in Macaques Is Dependent on Superior Dorsolateral Prefrontal Cortex But Not Orbitofrontal Cortex , 2019, The Journal of Neuroscience.

[5]  Adam Kepecs,et al.  The Neurobiology of Confidence: From Beliefs to Neurons. , 2019, Cold Spring Harbor symposia on quantitative biology.

[6]  S. Fleming,et al.  Thinking about thinking: A coordinate-based meta-analysis of neuroimaging studies of metacognitive judgements , 2018, Brain and neuroscience advances.

[7]  Lars Muckli,et al.  The Predictive Coding Account of Psychosis , 2018, Biological Psychiatry.

[8]  Loren M. Frank,et al.  The hippocampal sharp wave–ripple in memory retrieval for immediate use and consolidation , 2018, Nature Reviews Neuroscience.

[9]  C. Gillan,et al.  Psychiatric Symptom Dimensions Are Associated With Dissociable Shifts in Metacognition but Not Task Performance , 2018, Biological Psychiatry.

[10]  Y. Miyashita,et al.  Reversible Silencing of the Frontopolar Cortex Selectively Impairs Metacognitive Judgment on Non-experience in Primates , 2018, Neuron.

[11]  Nader Pouratian,et al.  Single-Neuron Representation of Memory Strength and Recognition Confidence in Left Human Posterior Parietal Cortex , 2018, Neuron.

[12]  John T Wixted,et al.  The Relationship Between Eyewitness Confidence and Identification Accuracy: A New Synthesis , 2017, Psychological science in the public interest : a journal of the American Psychological Society.

[13]  S. Eisenacher,et al.  The Importance of Metamemory Functioning to the Pathogenesis of Psychosis , 2017, Front. Psychol..

[14]  Adam Kepecs,et al.  Midbrain Dopamine Neurons Signal Belief in Choice Accuracy during a Perceptual Decision , 2017, Current Biology.

[15]  Yasushi Miyashita,et al.  Causal neural network of metamemory for retrospection in primates , 2017, Science.

[16]  S. Kouider,et al.  Behavioral and Neural Indices of Metacognitive Sensitivity in Preverbal Infants , 2016, Current Biology.

[17]  Ádám Kepecs,et al.  A mathematical framework for statistical decision confidence , 2015, bioRxiv.

[18]  Joshua I. Sanders,et al.  Signatures of a Statistical Computation in the Human Sense of Confidence , 2016, Neuron.

[19]  Alexandre Pouget,et al.  Confidence and certainty: distinct probabilistic quantities for different goals , 2016, Nature Neuroscience.

[20]  B. Mensh,et al.  Emotor control: computations underlying bodily resource allocation, emotions, and confidence , 2015, Dialogues in clinical neuroscience.

[21]  Yadin Dudai,et al.  The Consolidation and Transformation of Memory , 2015, Neuron.

[22]  M. Sigman,et al.  Confidence as Bayesian Probability: From Neural Origins to Behavior , 2015, Neuron.

[23]  Hakwan Lau,et al.  There are things that we know that we know, and there are things that we do not know we do not know: Confidence in decision-making , 2015, Neuroscience & Biobehavioral Reviews.

[24]  U. Rutishauser,et al.  Representation of retrieval confidence by single neurons in the human medial temporal lobe , 2015, Nature Neuroscience.

[25]  Heidi L. Marsh,et al.  Information seeking in capuchins (Cebus apella): A rudimentary form of metacognition? , 2015, Animal Cognition.

[26]  A. Koulakov,et al.  Orbitofrontal Cortex Is Required for Optimal Waiting Based on Decision Confidence , 2014, Neuron.

[27]  A. Radomsky,et al.  When more is less: doubt, repetition, memory, metamemory, and compulsive checking in OCD. , 2014, Behaviour research and therapy.

[28]  G. Buzsáki,et al.  The log-dynamic brain: how skewed distributions affect network operations , 2014, Nature Reviews Neuroscience.

[29]  Michael N. Shadlen,et al.  Effects of Cortical Microstimulation on Confidence in a Perceptual Decision , 2014, Neuron.

[30]  Clint J. Perry,et al.  Honey bees selectively avoid difficult choices , 2013, Proceedings of the National Academy of Sciences.

[31]  A. Pouget,et al.  Probabilistic brains: knowns and unknowns , 2013, Nature Neuroscience.

[32]  Yutaka Komura,et al.  Responses of pulvinar neurons reflect a subject's confidence in visual categorization , 2013, Nature Neuroscience.

[33]  Paul G. Middlebrooks,et al.  Neuronal Correlates of Metacognition in Primate Frontal Cortex , 2012, Neuron.

[34]  R. Dolan,et al.  Knowing how much you don't know: a neural organization of uncertainty estimates , 2012, Nature Reviews Neuroscience.

[35]  Adam Kepecs,et al.  A computational framework for the study of confidence in humans and animals , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[36]  Christopher Summerfield,et al.  Metacognition in human decision-making: confidence and error monitoring , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[37]  A. Yonelinas,et al.  Recollection and familiarity: Examining controversial assumptions and new directions , 2010, Hippocampus.

[38]  N. Emery Cognition, Evolution, and Behavior Cognition, Evolution, and Behavior. 2nd edn. By Sara J. Shettleworth. Oxford: Oxford University Press (2009). Pp. xiii+700. Price $59.95 paperback. , 2010, Animal Behaviour.

[39]  J. Wixted,et al.  A continuous dual-process model of remember/know judgments. , 2010, Psychological review.

[40]  J. D. Smith The study of animal metacognition , 2009, Trends in Cognitive Sciences.

[41]  K. Jellinger,et al.  The Missing Link in Cognition. Origins of self-reflective consciousness , 2009 .

[42]  M. Shadlen,et al.  Representation of Confidence Associated with a Decision by Neurons in the Parietal Cortex , 2009, Science.

[43]  W. Newsome,et al.  The Trouble with Choice: Studying Decision Variables in the Brain , 2009 .

[44]  Hatim A. Zariwala,et al.  Neural correlates, computation and behavioural impact of decision confidence , 2008, Nature.

[45]  Peter Carruthers,et al.  Meta-cognition in Animals: A Skeptical Look , 2008 .

[46]  Alfred W. Kaszniak,et al.  Metamemory Experiments in Neurological Populations: A Review , 2005, Neuropsychology Review.

[47]  W. Newsome,et al.  Matching Behavior and the Representation of Value in the Parietal Cortex , 2004, Science.

[48]  R. Hampton Rhesus monkeys know when they remember , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[49]  A. Dickinson,et al.  Episodic-like memory during cache recovery by scrub jays , 1998, Nature.

[50]  L. Cooper,et al.  Memory for temporal order of new and familiar spatial location sequences: role of the medial prefrontal cortex. , 1997, Learning & memory.

[51]  H. de Wit,et al.  Determination of discount functions in rats with an adjusting-amount procedure. , 1997, Journal of the experimental analysis of behavior.

[52]  J. D. Smith,et al.  The uncertain response in the bottlenosed dolphin (Tursiops truncatus). , 1995, Journal of experimental psychology. General.

[53]  M. Commons The effect of delay and of intervening events on reinforcement value , 2013 .

[54]  E. Balint Memory and consciousness. , 1987, The International journal of psycho-analysis.

[55]  J. M. Novak,et al.  Serial position curve in rats: role of the dorsal hippocampus. , 1982, Science.