Is There Neural Evidence for an Evidence Accumulation Process in Memory Decisions?

Models of evidence accumulation have been very successful at describing human decision making behavior. Recent years have also seen the first reports of neural correlates of this accumulation process. However, these studies have mostly focused on perceptual decision making tasks, ignoring the role of additional cognitive processes like memory retrieval that are crucial in real-world decisions. In this study, we tried to find a neural signature of evidence accumulation during a recognition memory task. To do this, we applied a method we have successfully used to localize evidence accumulation in scalp EEG during a perceptual decision making task. This time, however, we applied it to intracranial EEG recordings, which provide a much higher spatial resolution. We identified several brain areas where activity ramps up over time, but these neural patterns do not appear to be modulated by behavioral variables such as the amount of available evidence or response time. This casts doubt on the idea of evidence accumulation as a general decision-making mechanism underlying different types of decisions.

[1]  M. K. van Vugt,et al.  EEG Oscillations Reveal Neural Correlates of Evidence Accumulation , 2012, Front. Neurosci..

[2]  T. Hothorn,et al.  Simultaneous Inference in General Parametric Models , 2008, Biometrical journal. Biometrische Zeitschrift.

[3]  S. Raghavachari,et al.  Gating of Human Theta Oscillations by a Working Memory Task , 2001, The Journal of Neuroscience.

[4]  D. Bates,et al.  Mixed-Effects Models in S and S-PLUS , 2001 .

[5]  R. Baayen,et al.  Mixed-effects modeling with crossed random effects for subjects and items , 2008 .

[6]  Brian Litt,et al.  Hippocampal gamma oscillations increase with working memory load , 2009 .

[7]  J. Gold,et al.  The neural basis of decision making. , 2007, Annual review of neuroscience.

[8]  Christian Büchel,et al.  Classic EEG motor potentials track the emergence of value-based decisions , 2013, NeuroImage.

[9]  Scott D. Brown,et al.  Domain General Mechanisms of Perceptual Decision Making in Human Cortex , 2009, The Journal of Neuroscience.

[10]  Jochen Ditterich,et al.  A Comparison between Mechanisms of Multi-Alternative Perceptual Decision Making: Ability to Explain Human Behavior, Predictions for Neurophysiology, and Relationship with Decision Theory , 2010, Front. Neurosci..

[11]  Michael J. Kahana,et al.  Direct brain recordings fuel advances in cognitive electrophysiology , 2010, Trends in Cognitive Sciences.

[12]  S. Kelly,et al.  A supramodal accumulation-to-bound signal that determines perceptual decisions in humans , 2012, Nature Neuroscience.

[13]  Kenneth A. Norman,et al.  How Inhibitory Oscillations Can Train Neural Networks and Punish Competitors , 2006, Neural Computation.

[14]  A. Pouget,et al.  Variance as a Signature of Neural Computations during Decision Making , 2011, Neuron.

[15]  R. Sekuler,et al.  Recognizing spatial patterns: a noisy exemplar approach , 2002, Vision Research.

[16]  M. Shadlen,et al.  Neural correlates of a decision in the dorsolateral prefrontal cortex of the macaque , 1999, Nature Neuroscience.

[17]  Michael X. Cohen,et al.  Reward expectation modulates feedback-related negativity and EEG spectra , 2007, NeuroImage.

[18]  Andreas K. Engel,et al.  Buildup of Choice-Predictive Activity in Human Motor Cortex during Perceptual Decision Making , 2009, Current Biology.

[19]  Elisabeth J. Ploran,et al.  Evidence Accumulation and the Moment of Recognition: Dissociating Perceptual Recognition Processes Using fMRI , 2007, The Journal of Neuroscience.

[20]  E. Wagenmakers,et al.  EZ does it! Extensions of the EZ-diffusion model , 2008, Psychonomic bulletin & review.

[21]  Clas Blomberg.  § 32 – THE NEURAL SYSTEM , 2007 .

[22]  Scott D. Brown,et al.  The simplest complete model of choice response time: Linear ballistic accumulation , 2008, Cognitive Psychology.

[23]  W. Newsome,et al.  Neural basis of a perceptual decision in the parietal cortex (area LIP) of the rhesus monkey. , 2001, Journal of neurophysiology.

[24]  James F. Cavanagh,et al.  Frontal theta links prediction errors to behavioral adaptation in reinforcement learning , 2010, NeuroImage.

[25]  M. Shadlen,et al.  A Neural Implementation of Wald’s Sequential Probability Ratio Test , 2015, Neuron.

[26]  Leslie G. Ungerleider,et al.  The neural systems that mediate human perceptual decision making , 2008, Nature Reviews Neuroscience.

[27]  M. Manosevitz.  High-Speed Scanning in Human Memory , .

[28]  Richard P. Heitz,et al.  Neurally constrained modeling of perceptual decision making. , 2010, Psychological review.

[29]  R. Nosofsky.  Tests of an exemplar model for relating perceptual classification and recognition memory. , 1991, Journal of experimental psychology. Human perception and performance.

[30]  James L. McClelland,et al.  The time course of perceptual choice: the leaky, competing accumulator model. , 2001, Psychological review.

[31]  Michael X. Cohen,et al.  Nuclei Accumbens Phase Synchrony Predicts Decision-Making Reversals Following Negative Feedback , 2009, The Journal of Neuroscience.

[32]  P. Fries.  A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

[33]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[34]  Ulman Lindenberger,et al.  Coordinated within-Trial Dynamics of Low-Frequency Neural Rhythms Controls Evidence Accumulation , 2014, The Journal of Neuroscience.

[35]  R. Sekuler,et al.  Intracranial electroencephalography reveals two distinct similarity effects during item recognition , 2009, Brain Research.

[36]  Miranda Robertson,et al.  Neural systems , 1977, Nature.

[37]  J. Gold,et al.  Caudate Encodes Multiple Computations for Perceptual Decisions , 2010, The Journal of Neuroscience.

[38]  Stanislas Dehaene,et al.  Accumulation of Evidence during Sequential Decision Making: The Importance of Top–Down Factors , 2010, The Journal of Neuroscience.

[39]  W. G. Workman,et al.  Suggestions for Simplifying the Computation of Vincent Curves , 1950 .

[40]  A. Pérez-Villalba.  Rhythms of the Brain, G. Buzsáki. Oxford University Press, Madison Avenue, New York (2006), Price: GB £42.00, p. 448, ISBN: 0-19-530106-4 , 2008 .

[41]  Roger Ratcliff,et al.  A Theory of Memory Retrieval. , 1978 .

[42]  Leslie G. Ungerleider,et al.  Involvement of human left dorsolateral prefrontal cortex in perceptual decision making is independent of response modality , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[43]  W T Newsome,et al.  Target selection for saccadic eye movements: prelude activity in the superior colliculus during a direction-discrimination task. , 2001, Journal of neurophysiology.

[44]  J. Henrich,et al.  Most people are not WEIRD , 2010, Nature.

[45]  Brian Litt,et al.  Behavioral / Systems / Cognitive Hippocampal Gamma Oscillations Increase with Memory Load , 2010 .

[46]  T. Womelsdorf,et al.  Human Neuroscience , 2022 .