Recurrent plasticity mechanisms for perceptual decisions in the human brain

Learning and experience are critical for making successful decisions in the face of inherently ambiguous and noisy information. Yet, the human brain computations that mediate this perceptual learning skill remain highly debated, as fMRI at standard resolution does not allow us to discern whether learning alters sensory encoding or top-down influences. Here, we capitalize on the sub-millimetre resolution of ultra-high field imaging to interrogate the finer-scale computations that mediate perceptual learning in the human brain. Combining 7T laminar imaging with orientation discrimination training, we demonstrate learning-dependent changes in superficial V1 layers, suggesting that training alters read-out rather than input signals in the visual cortex. Further, training enhances feedforward connectivity between superficial V1 layers and middle layers of posterior parietal cortex. Our findings propose that the brain learns to translate sensory information to perceptual decisions via recurrent processing within visual cortex and enhanced connectivity from sensory to decision-related areas.

[1]  C. Gilbert,et al.  The Neural Basis of Perceptual Learning , 2001, Neuron.

[2]  N. Qian,et al.  Learning and adaptation in a recurrent model of V1 orientation selectivity. , 2003, Journal of neurophysiology.

[3]  Liang Wang,et al.  Probabilistic Maps of Visual Topography in Human Cortex. , 2015, Cerebral cortex.

[4]  Lars Muckli,et al.  A Perspective on Cortical Layering and Layer-Spanning Neuronal Elements , 2018, Front. Neuroanat..

[5]  J. Maunsell,et al.  The Effect of Perceptual Learning on Neuronal Responses in Monkey Visual Area V4 , 2004, The Journal of Neuroscience.

[6]  Nikos K. Logothetis,et al.  fMRI at High Spatial Resolution: Implications for BOLD-Models , 2016, Front. Comput. Neurosci..

[7]  C. Furmanski,et al.  Learning Strengthens the Response of Primary Visual Cortex to Simple Patterns , 2004, Current Biology.

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

[9]  T. Wiesel,et al.  Clustered intrinsic connections in cat visual cortex , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  Harald E. Möller,et al.  Non-BOLD contrast for laminar fMRI in humans: CBF, CBV, and CMRO2 , 2017, NeuroImage.

[11]  Aaron R. Seitz,et al.  Towards a whole brain model of Perceptual Learning , 2018, Current Opinion in Behavioral Sciences.

[12]  A. Grinvald,et al.  Relationship between intrinsic connections and functional architecture revealed by optical imaging and in vivo targeted biocytin injections in primate striate cortex. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[13]  G. Glover,et al.  Retinotopic organization in human visual cortex and the spatial precision of functional MRI. , 1997, Cerebral cortex.

[14]  Klaus Obermayer,et al.  Adaptivity of Tuning Functions in a Generic Recurrent Network Model of a Cortical Hypercolumn , 2005, The Journal of Neuroscience.

[15]  Pieter R. Roelfsema,et al.  Distinct Roles of the Cortical Layers of Area V1 in Figure-Ground Segregation , 2013, Current Biology.

[16]  Robert Turner,et al.  Resolving multisensory and attentional influences across cortical depth in sensory cortices , 2019, bioRxiv.

[17]  Nikola T. Markov,et al.  Anatomy of hierarchy: Feedforward and feedback pathways in macaque visual cortex , 2013, The Journal of comparative neurology.

[18]  S. Klein,et al.  Rule-Based Learning Explains Visual Perceptual Learning and Its Specificity and Transfer , 2010, The Journal of Neuroscience.

[19]  C. Gilbert,et al.  Adult Visual Cortical Plasticity , 2012, Neuron.

[20]  Zoe Kourtzi,et al.  Training Transfers the Limits on Perception from Parietal to Ventral Cortex , 2014, Current Biology.

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

[22]  Taiyong Bi,et al.  Sharpened cortical tuning and enhanced cortico-cortical communication contribute to the long-term neural mechanisms of visual motion perceptual learning , 2015, NeuroImage.

[23]  David J. Heeger,et al.  Non-commercial Research and Educational Use including without Limitation Use in Instruction at Your Institution, Sending It to Specific Colleagues That You Know, and Providing a Copy to Your Institution's Administrator. All Other Uses, Reproduction and Distribution, including without Limitation Comm , 2022 .

[24]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

[25]  John T. Serences,et al.  Exploring the relationship between perceptual learning and top-down attentional control , 2012, Vision Research.

[26]  D. Tanné,et al.  Perceptual learning: learning to see , 1994, Current Opinion in Neurobiology.

[27]  Aaron R. Seitz,et al.  Prolonged Training at Threshold Promotes Robust Retinotopic Specificity in Perceptual Learning , 2014, The Journal of Neuroscience.

[28]  Pieter R. Roelfsema,et al.  Benchmarking laminar fMRI: Neuronal spiking and synaptic activity during top-down and bottom-up processing in the different layers of cortex , 2017, NeuroImage.

[29]  G. Orban,et al.  Learning to See the Difference Specifically Alters the Most Informative V4 Neurons , 2006, The Journal of Neuroscience.

[30]  Dimo Ivanov,et al.  Impact of acquisition and analysis strategies on cortical depth-dependent fMRI , 2017, NeuroImage.

[31]  G. Orban,et al.  Practising orientation identification improves orientation coding in V1 neurons , 2001, Nature.

[32]  L. Toth,et al.  How accurate is magnetic resonance imaging of brain function? , 2003, Trends in Neurosciences.

[33]  Essa Yacoub,et al.  High resolution data analysis strategies for mesoscale human functional MRI at 7 and 9.4 T , 2018, NeuroImage.

[34]  M. Corbetta,et al.  Learning sculpts the spontaneous activity of the resting human brain , 2009, Proceedings of the National Academy of Sciences.

[35]  Bryan M. Hooks,et al.  Circuitry Underlying Experience-Dependent Plasticity in the Mouse Visual System , 2020, Neuron.

[36]  P. Maquet,et al.  Neural correlates of perceptual learning: A functional MRI study of visual texture discrimination , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Essa Yacoub,et al.  Multivoxel Pattern of Blood Oxygen Level Dependent Activity can be sensitive to stimulus specific fine scale responses , 2019, bioRxiv.

[38]  H. Duvernoy,et al.  Cortical blood vessels of the human brain , 1981, Brain Research Bulletin.

[39]  Ovidiu Lungu,et al.  Consolidation alters motor sequence-specific distributed representations , 2018, bioRxiv.

[40]  Lin Yang,et al.  Perceptual Learning Increases the Strength of the Earliest Signals in Visual Cortex , 2010, The Journal of Neuroscience.

[41]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[42]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[43]  Lawrence L. Wald,et al.  Laminar analysis of 7T BOLD using an imposed spatial activation pattern in human V1 , 2010, NeuroImage.

[44]  Yuka Sasaki,et al.  Perceptual learning: toward a comprehensive theory. , 2015, Annual review of psychology.

[45]  C. Gilbert,et al.  Perceptual learning and adult cortical plasticity , 2009, The Journal of physiology.

[46]  G. Orban,et al.  Human perceptual learning in identifying the oblique orientation: retinotopy, orientation specificity and monocularity. , 1995, The Journal of physiology.

[47]  Kamil Ugurbil,et al.  A critical assessment of data quality and venous effects in sub-millimeter fMRI , 2019, NeuroImage.

[48]  David G Norris,et al.  Dissociable laminar profiles of concurrent bottom-up and top-down modulation in the human visual cortex , 2018, bioRxiv.

[49]  R. Douglas,et al.  Recurrent neuronal circuits in the neocortex , 2007, Current Biology.

[50]  R. Shapley,et al.  Orientation Selectivity in Macaque V1: Diversity and Laminar Dependence , 2002, The Journal of Neuroscience.

[51]  Frank Tong,et al.  Perceptual Learning Selectively Refines Orientation Representations in Early Visual Cortex , 2012, The Journal of Neuroscience.

[52]  Lucy S. Petro,et al.  Contextual Feedback to Superficial Layers of V1 , 2015, Current Biology.

[53]  Pierre-Louis Bazin,et al.  Anatomically motivated modeling of cortical laminae , 2014, NeuroImage.

[54]  S. Hochstein,et al.  The reverse hierarchy theory of visual perceptual learning , 2004, Trends in Cognitive Sciences.

[55]  R. Desimone,et al.  Laminar differences in gamma and alpha coherence in the ventral stream , 2011, Proceedings of the National Academy of Sciences.

[56]  Essa Yacoub,et al.  Signal and noise characteristics of Hahn SE and GE BOLD fMRI at 7 T in humans , 2005, NeuroImage.

[57]  Z. Kourtzi,et al.  Learning Alters the Tuning of Functional Magnetic Resonance Imaging Patterns for Visual Forms , 2010, The Journal of Neuroscience.

[58]  B. Dosher,et al.  Visual Perceptual Learning and Models. , 2017, Annual review of vision science.

[59]  A. M. Dale,et al.  BORDERS OF MULTIPLE VISUAL AREAS IN HUMANS REVEALED BY FUNCTIONAL MRI , 1995 .

[60]  Sharon L. Thompson-Schill,et al.  Using Informational Connectivity to Measure the Synchronous Emergence of fMRI Multi-voxel Information Across Time , 2014, Journal of visualized experiments : JoVE.

[61]  P. Goldman-Rakic,et al.  Preface: Cerebral Cortex Has Come of Age , 1991 .

[62]  Ikuko Mukai,et al.  Behavioral/systems/cognitive Activations in Visual and Attention-related Areas Predict and Correlate with the Degree of Perceptual Learning , 2022 .

[63]  J. Haynes,et al.  Perceptual Learning and Decision-Making in Human Medial Frontal Cortex , 2011, Neuron.

[64]  K. Rockland,et al.  Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey , 1979, Brain Research.

[65]  Bruce Fischl,et al.  Accurate and robust brain image alignment using boundary-based registration , 2009, NeuroImage.

[66]  Si Wu,et al.  Perceptual training continuously refines neuronal population codes in primary visual cortex , 2014, Nature Neuroscience.

[67]  J W Belliveau,et al.  Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. , 1995, Science.

[68]  Haynes John-Dylan,et al.  Perceptual learning and decision making in human medial frontal cortex , 2012 .

[69]  Steen Moeller,et al.  Multiband multislice GE‐EPI at 7 tesla, with 16‐fold acceleration using partial parallel imaging with application to high spatial and temporal whole‐brain fMRI , 2010, Magnetic resonance in medicine.

[70]  Martin J. Chadwick,et al.  Big-Loop Recurrence within the Hippocampal System Supports Integration of Information across Episodes , 2018, Neuron.

[71]  R. Goebel,et al.  Frequency preference and attention effects across cortical depths in the human primary auditory cortex , 2015, Proceedings of the National Academy of Sciences.

[72]  S. Hochstein,et al.  Task difficulty and the specificity of perceptual learning , 1997, Nature.

[73]  Marc N. Coutanche,et al.  Beyond Functional Connectivity: Investigating Networks of Multivariate Representations , 2018, Trends in Cognitive Sciences.

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

[75]  Kamil Ugurbil,et al.  An integrative model for neuronal activity-induced signal changes for gradient and spin echo functional imaging , 2009, NeuroImage.