A Probability Distribution over Latent Causes, in the Orbitofrontal Cortex

The orbitofrontal cortex (OFC) has been implicated in both the representation of “state,” in studies of reinforcement learning and decision making, and also in the representation of “schemas,” in studies of episodic memory. Both of these cognitive constructs require a similar inference about the underlying situation or “latent cause” that generates our observations at any given time. The statistically optimal solution to this inference problem is to use Bayes' rule to compute a posterior probability distribution over latent causes. To test whether such a posterior probability distribution is represented in the OFC, we tasked human participants with inferring a probability distribution over four possible latent causes, based on their observations. Using fMRI pattern similarity analyses, we found that BOLD activity in the OFC is best explained as representing the (log-transformed) posterior distribution over latent causes. Furthermore, this pattern explained OFC activity better than other task-relevant alternatives, such as the most probable latent cause, the most recent observation, or the uncertainty over latent causes. SIGNIFICANCE STATEMENT Our world is governed by hidden (latent) causes that we cannot observe, but which generate the observations we see. A range of high-level cognitive processes require inference of a probability distribution (or “belief distribution”) over the possible latent causes that might be generating our current observations. This is true for reinforcement learning and decision making (where the latent cause comprises the true “state” of the task), and for episodic memory (where memories are believed to be organized by the inferred situation or “schema”). Using fMRI, we show that this belief distribution over latent causes is encoded in patterns of brain activity in the orbitofrontal cortex, an area that has been separately implicated in the representations of both states and schemas.

[1]  Robert Tibshirani,et al.  Bootstrap Methods for Standard Errors, Confidence Intervals, and Other Measures of Statistical Accuracy , 1986 .

[2]  I. Erev,et al.  On adaptation, maximization, and reinforcement learning among cognitive strategies. , 2005, Psychological review.

[3]  L. Maloney,et al.  Neural Mechanisms for Integrating Prior Knowledge and Likelihood in Value-Based Probabilistic Inference , 2015, Journal of Neuroscience.

[4]  Dorothy Tse,et al.  Schema-Dependent Gene Activation and Memory Encoding in Neocortex , 2011, Science.

[5]  Robert C. Wilson,et al.  Orbitofrontal Cortex as a Cognitive Map of Task Space , 2014, Neuron.

[6]  M. Gluck,et al.  How do people solve the "weather prediction" task?: individual variability in strategies for probabilistic category learning. , 2002, Learning & memory.

[7]  Vanessa E. Ghosh,et al.  What is a memory schema? A historical perspective on current neuroscience literature , 2014, Neuropsychologia.

[8]  Margaret L. Schlichting,et al.  Memory integration: neural mechanisms and implications for behavior , 2015, Current Opinion in Behavioral Sciences.

[9]  D. Blei,et al.  Context, learning, and extinction. , 2010, Psychological review.

[10]  R Turner,et al.  Optimized EPI for fMRI studies of the orbitofrontal cortex , 2003, NeuroImage.

[11]  C. Koch,et al.  Multiplicative computation in a visual neuron sensitive to looming , 2002, Nature.

[12]  Y. Niv,et al.  Learning latent structure: carving nature at its joints , 2010, Current Opinion in Neurobiology.

[13]  Amos Storkey,et al.  Advances in Neural Information Processing Systems 20 , 2007 .

[14]  J. Gold,et al.  Banburismus and the Brain Decoding the Relationship between Sensory Stimuli, Decisions, and Reward , 2002, Neuron.

[15]  M Konishi,et al.  Auditory Spatial Receptive Fields Created by Multiplication , 2001, Science.

[16]  D. Tank,et al.  Dendritic Integration in Mammalian Neurons, a Century after Cajal , 1996, Neuron.

[17]  Alexander Borst,et al.  How does Nature Program Neuron Types? , 2008, Front. Neurosci..

[18]  Nir Vulkan An Economist's Perspective on Probability Matching , 2000 .

[19]  Nikolaus Kriegeskorte,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

[20]  Dorothy Tse,et al.  References and Notes Supporting Online Material Materials and Methods Figs. S1 to S5 Tables S1 to S3 Electron Impact (ei) Mass Spectra Chemical Ionization (ci) Mass Spectra References Schemas and Memory Consolidation Research Articles Research Articles Research Articles Research Articles , 2022 .

[21]  David S. Touretzky,et al.  Model Uncertainty in Classical Conditioning , 2003, NIPS.

[22]  Michael N. Shadlen,et al.  Probabilistic reasoning by neurons , 2007, Nature.

[23]  J. Gibbon Scalar expectancy theory and Weber's law in animal timing. , 1977 .

[24]  Mathieu d'Acremont,et al.  Activity in Inferior Parietal and Medial Prefrontal Cortex Signals the Accumulation of Evidence in a Probability Learning Task , 2013, PLoS Comput. Biol..

[25]  Leslie Pack Kaelbling,et al.  Planning and Acting in Partially Observable Stochastic Domains , 1998, Artif. Intell..

[26]  Adam Santoro,et al.  Patterns across multiple memories are identified over time , 2014, Nature Neuroscience.

[27]  Stella F. Lourenco,et al.  Spatial attention and the mental number line: Evidence for characteristic biases and compression , 2007, Neuropsychologia.

[28]  J. O'Doherty,et al.  Reward Value Coding Distinct From Risk Attitude-Related Uncertainty Coding in Human Reward Systems , 2006, Journal of neurophysiology.

[29]  Anders M. Dale,et al.  Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature , 2010, NeuroImage.

[30]  L. Davachi,et al.  What Constitutes an Episode in Episodic Memory? , 2011, Psychological science.

[31]  H. Critchley,et al.  Neural Activity in the Human Brain Relating to Uncertainty and Arousal during Anticipation , 2001, Neuron.

[32]  A. Hupbach,et al.  The dynamics of memory: context-dependent updating. , 2008, Learning & memory.

[33]  R. Henson,et al.  How schema and novelty augment memory formation , 2012, Trends in Neurosciences.

[34]  Hugo L. Fernandes,et al.  Differential Representations of Prior and Likelihood Uncertainty in the Human Brain , 2012, Current Biology.

[35]  Arne D. Ekstrom,et al.  Differential Connectivity of Perirhinal and Parahippocampal Cortices within Human Hippocampal Subregions Revealed by High-Resolution Functional Imaging , 2012, The Journal of Neuroscience.

[36]  C. Ranganath,et al.  Two cortical systems for memory-guided behaviour , 2012, Nature Reviews Neuroscience.

[37]  Jennifer A. Mangels,et al.  A Neostriatal Habit Learning System in Humans , 1996, Science.