Projections of non-invasive human recordings into state space show unfolding of spontaneous and over-trained choice

Choices rely on a transformation of sensory inputs into motor responses. Using invasive single neuron recordings, the evolution of a choice process has been tracked by projecting population neural responses into state spaces. Here we develop an approach that allows us to recover state space trajectories on a millisecond timescale in non-invasive human recordings. We selectively suppress activity related to relevant and irrelevant sensory inputs and response direction in magnetoencephalography data acquired during context-dependent choices. Recordings from premotor cortex show a smooth progression from sensory input encoding to response encoding. In contrast to previous macaque recordings, information related to choice-irrelevant features is represented more weakly than choice-relevant sensory information. To test whether this mechanistic difference between species is caused by extensive overtraining common in non-human primate studies, we trained humans on >20,000 trials of the task. Choice-irrelevant features were still weaker than relevant features in premotor cortex after overtraining.

[1]  Jonathon Love,et al.  JASP: Graphical Statistical Software for Common Statistical Designs , 2019, Journal of Statistical Software.

[2]  Laurence T. Hunt,et al.  Triple Dissociation of Attention and Decision Computations across Prefrontal Cortex , 2017, Nature Neuroscience.

[3]  F. D. Lange,et al.  How Do Expectations Shape Perception? , 2018, Trends in Cognitive Sciences.

[4]  Matthew F.S. Rushworth,et al.  Contrasting Roles for Orbitofrontal Cortex and Amygdala in Credit Assignment and Learning in Macaques , 2015, Neuron.

[5]  Ari S. Morcos,et al.  History-dependent variability in population dynamics during evidence accumulation in cortex , 2016, Nature Neuroscience.

[6]  J. Gold,et al.  Visual Decision-Making in an Uncertain and Dynamic World. , 2017, Annual review of vision science.

[7]  Timothy E. J. Behrens,et al.  Online evaluation of novel choices by simultaneous representation of multiple memories , 2013, Nature Neuroscience.

[8]  P. Sachs,et al.  SMARCAD1 ATPase activity is required to silence endogenous retroviruses in embryonic stem cells , 2019, Nature Communications.

[9]  Marius Usher,et al.  The Timescale of Perceptual Evidence Integration Can Be Adapted to the Environment , 2013, Current Biology.

[10]  Mark W. Woolrich,et al.  How reliable are MEG resting-state connectivity metrics? , 2016, NeuroImage.

[11]  R. Yuste From the neuron doctrine to neural networks , 2015, Nature Reviews Neuroscience.

[12]  Keiji Tanaka,et al.  Matching Categorical Object Representations in Inferior Temporal Cortex of Man and Monkey , 2008, Neuron.

[13]  Christian F. Doeller,et al.  Evidence for grid cells in a human memory network , 2010, Nature.

[14]  N. Kanwisher,et al.  fMRI Adaptation Reveals Mirror Neurons in Human Inferior Parietal Cortex , 2008, Current Biology.

[15]  E. Miller,et al.  Response to Comment on "Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices" , 2007, Science.

[16]  Floris P de Lange,et al.  Prior expectations induce prestimulus sensory templates , 2017, Proceedings of the National Academy of Sciences.

[17]  Timothy Edward John Behrens,et al.  Segregated Encoding of Reward–Identity and Stimulus–Reward Associations in Human Orbitofrontal Cortex , 2013, The Journal of Neuroscience.

[18]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[19]  G L Gerstein,et al.  Single-unit activity in temporal association cortex of the monkey. , 1967, Journal of neurophysiology.

[20]  J. Duncan,et al.  Competitive brain activity in visual attention , 1997, Current Opinion in Neurobiology.

[21]  N. P. Bichot,et al.  Visual feature selectivity in frontal eye fields induced by experience in mature macaques , 1996, Nature.

[22]  Floris P de Lange,et al.  Statistical learning attenuates visual activity only for attended stimuli , 2019, bioRxiv.

[23]  Miriam C Klein-Flügge,et al.  Multiple associative structures created by reinforcement and incidental statistical learning mechanisms , 2019, Nature Communications.

[24]  Karl J. Friston,et al.  Predictive coding under the free-energy principle , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[25]  Matthew J. Brookes,et al.  Beamformer reconstruction of correlated sources using a modified source model , 2007, NeuroImage.

[26]  Nicholas A. Steinmetz,et al.  Top-down control of visual attention , 2010, Current Opinion in Neurobiology.

[27]  Timothy E. J. Behrens,et al.  Capturing the temporal evolution of choice across prefrontal cortex , 2015, eLife.

[28]  T. Egner,et al.  Cognitive control mechanisms resolve conflict through cortical amplification of task-relevant information , 2005, Nature Neuroscience.

[29]  Matthew T. Kaufman,et al.  A category-free neural population supports evolving demands during decision-making , 2014, Nature Neuroscience.

[30]  Mark W. Woolrich,et al.  A symmetric multivariate leakage correction for MEG connectomes , 2015, NeuroImage.

[31]  Tirin Moore,et al.  Prefrontal contributions to visual selective attention. , 2013, Annual review of neuroscience.

[32]  Armin Brandt,et al.  Neural Activity in Human Hippocampal Formation Reveals the Spatial Context of Retrieved Memories , 2013, Science.

[33]  F. D. Lange,et al.  Selective Activation of the Deep Layers of the Human Primary Visual Cortex by Top-Down Feedback , 2016, Current Biology.

[34]  C. Elger,et al.  Human memory formation is accompanied by rhinal–hippocampal coupling and decoupling , 2001, Nature Neuroscience.

[35]  Mark W. Woolrich,et al.  MEG beamforming using Bayesian PCA for adaptive data covariance matrix regularization , 2011, NeuroImage.

[36]  W. Newsome,et al.  Context-dependent computation by recurrent dynamics in prefrontal cortex , 2013, Nature.

[37]  Floris P. de Lange,et al.  Statistical learning attenuates visual activity only for attended stimuli , 2019 .

[38]  Adam Gazzaley,et al.  Functional interactions between prefrontal and visual association cortex contribute to top-down modulation of visual processing. , 2007, Cerebral cortex.

[39]  Joshua I. Gold,et al.  Shared Mechanisms of Perceptual Learning and Decision Making , 2010, Top. Cogn. Sci..

[40]  Bolton K. H. Chau,et al.  The macaque anterior cingulate cortex translates counterfactual choice value into actual behavioral change , 2018, Nature Neuroscience.

[41]  E. Spelke,et al.  This Review Comes from a Themed Issue on Biocatalysis and Biotransformation Edited , 2022 .

[42]  Joseph W Kable,et al.  Normative evidence accumulation in unpredictable environments , 2015, eLife.

[43]  A. Borst Seeing smells: imaging olfactory learning in bees , 1999, Nature Neuroscience.

[44]  J. Duncan,et al.  Filtering of neural signals by focused attention in the monkey prefrontal cortex , 2002, Nature Neuroscience.

[45]  Richard N Henson,et al.  Repetition suppression to faces in the fusiform face area: A personal and dynamic journey , 2016, Cortex.

[46]  S. Hochstein,et al.  View from the Top Hierarchies and Reverse Hierarchies in the Visual System , 2002, Neuron.

[47]  Mark G. Stokes,et al.  Dynamic Brain States for Preparatory Attention and Working Memory , 2014 .

[48]  C. Summerfield,et al.  Expectation in perceptual decision making: neural and computational mechanisms , 2014, Nature Reviews Neuroscience.

[49]  Byron M. Yu,et al.  Dimensionality reduction for large-scale neural recordings , 2014, Nature Neuroscience.

[50]  Craig G. Richter,et al.  Top-Down Beta Enhances Bottom-Up Gamma , 2016, The Journal of Neuroscience.

[51]  Timothy Edward John Behrens,et al.  Unmasking Latent Inhibitory Connections in Human Cortex to Reveal Dormant Cortical Memories , 2016, Neuron.

[52]  Arne D. Ekstrom,et al.  Cellular networks underlying human spatial navigation , 2003, Nature.

[53]  M. D Rugg,et al.  The effect of repetition lag on electrophysiological and haemodynamic correlates of visual object priming , 2004, NeuroImage.

[54]  Nuo Li,et al.  Robust neuronal dynamics in premotor cortex during motor planning , 2016, Nature.

[55]  David Ardia,et al.  Generalized Autoregressive Score Models in R: The GAS Package , 2016, Journal of Statistical Software.

[56]  Zeb Kurth-Nelson,et al.  Learning-Induced Plasticity in Medial Prefrontal Cortex Predicts Preference Malleability , 2015, Neuron.

[57]  Markus Siegel,et al.  Cortical information flow during flexible sensorimotor decisions , 2015, Science.

[58]  Samuel J. D. Lawrence,et al.  Temporal tuning of repetition suppression across the visual cortex , 2019, bioRxiv.

[59]  M. Woolrich,et al.  Mechanisms underlying cortical activity during value-guided choice , 2011, Nature Neuroscience.

[60]  Matthew T. Kaufman,et al.  Neural population dynamics during reaching , 2012, Nature.

[61]  Christopher D. Harvey,et al.  Choice-specific sequences in parietal cortex during a virtual-navigation decision task , 2012, Nature.

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

[63]  Tirin Moore,et al.  Selective Attention from Voluntary Control of Neurons in Prefrontal Cortex , 2011, Science.

[64]  Samuel J. D. Lawrence,et al.  Temporal tuning of repetition suppression across the visual cortex. , 2019, Journal of neurophysiology.

[65]  S. Dehaene,et al.  A Magnitude Code Common to Numerosities and Number Symbols in Human Intraparietal Cortex , 2007, Neuron.

[66]  Raymond J Dolan,et al.  A map of abstract relational knowledge in the human hippocampal–entorhinal cortex , 2017, eLife.

[67]  Christos Constantinidis,et al.  Stable population coding for working memory coexists with heterogeneous neural dynamics in prefrontal cortex , 2016, Proceedings of the National Academy of Sciences.

[68]  Helen C. Barron,et al.  Repetition suppression: a means to index neural representations using BOLD? , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[69]  Karl J. Friston,et al.  A theory of cortical responses , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[70]  Jonathan Miller,et al.  Phase-tuned neuronal firing encodes human contextual representations for navigational goals , 2017, bioRxiv.

[71]  Jeffrey N. Rouder,et al.  Default Bayes factors for ANOVA designs , 2012 .

[72]  H. Kennedy,et al.  Alpha-Beta and Gamma Rhythms Subserve Feedback and Feedforward Influences among Human Visual Cortical Areas , 2016, Neuron.

[73]  Matthew T. Kaufman,et al.  Supplementary materials for : Cortical activity in the null space : permitting preparation without movement , 2014 .

[74]  U. Rutishauser,et al.  Human memory strength is predicted by theta-frequency phase-locking of single neurons , 2010, Nature.

[75]  R. Desimone,et al.  Neural mechanisms of selective visual attention. , 1995, Annual review of neuroscience.

[76]  N. P. Bichot,et al.  Effects of similarity and history on neural mechanisms of visual selection , 1999, Nature Neuroscience.

[77]  C. Law,et al.  Neural correlates of perceptual learning in a sensory-motor, but not a sensory, cortical area , 2008, Nature Neuroscience.

[78]  A. Todorović,et al.  Repetition Suppression and Expectation Suppression Are Dissociable in Time in Early Auditory Evoked Fields , 2012, The Journal of Neuroscience.

[79]  Jason P. Mitchell,et al.  Repetition suppression of ventromedial prefrontal activity during judgments of self and others , 2008, Proceedings of the National Academy of Sciences.