Perceptual Learning of Contrast Detection in the Human Lateral Geniculate Nucleus

The brain is continuously modified by perceptual experience throughout life. Perceptual learning, which refers to the long-term performance improvement resulting from practice, has been widely used as a paradigm to study experience-dependent brain plasticity in adults [1, 2]. In the visual system, adult plasticity is largely believed to be restricted to the cortex, with subcortical structures losing their capacity for change after a critical period of development [3, 4]. Although various cortical mechanisms have been shown to mediate visual perceptual learning [5-12], there has been no reported investigation of perceptual learning in subcortical nuclei. Here, human subjects were trained on a contrast detection task for 30 days, leading to a significant contrast sensitivity improvement that was specific to the trained eye and the trained visual hemifield. Training also resulted in an eye- and hemifield-specific fMRI signal increase to low-contrast patterns in the magnocellular layers of the lateral geniculate nucleus (LGN), even when subjects did not pay attention to the patterns. Such an increase was absent in the parvocellular layers of the LGN and visual cortical areas. Furthermore, the behavioral benefit significantly correlated with the neural enhancement. These findings suggest that LGN signals can be amplified by training to detect faint patterns. Neural plasticity induced by perceptual learning in human adults might not be confined to the cortical level but might occur as early as at the thalamic level.

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

[2]  Chang-Bing Huang,et al.  Perceptual Learning Improves Contrast Sensitivity of V1 Neurons in Cats , 2010, Current Biology.

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

[4]  K. H. Britten,et al.  Neuronal plasticity that underlies improvement in perceptual performance. , 1994, Science.

[5]  D Sagi,et al.  Where practice makes perfect in texture discrimination: evidence for primary visual cortex plasticity. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Tiangang Zhou,et al.  Perceptual learning modifies the functional specializations of visual cortical areas , 2016, Proceedings of the National Academy of Sciences.

[7]  A. Derrington The lateral geniculate nucleus , 2001, Current Biology.

[8]  R. Gattass,et al.  Laminar, columnar and topographic aspects of ocular dominance in the primary visual cortex ofCebus monkeys , 1992, Experimental Brain Research.

[9]  Paul T. Sowden,et al.  Perceptual learning of luminance contrast detection: specific for spatial frequency and retinal location but not orientation , 2002, Vision Research.

[10]  D. Buonomano,et al.  Cortical plasticity: from synapses to maps. , 1998, Annual review of neuroscience.

[11]  W. Martin Usrey,et al.  Rapid Plasticity of Visual Responses in the Adult Lateral Geniculate Nucleus , 2011, Neuron.

[12]  B. Dosher,et al.  An integrated reweighting theory of perceptual learning , 2013, Proceedings of the National Academy of Sciences.

[13]  Hao Zhou,et al.  Layer-specific response properties of the human lateral geniculate nucleus and superior colliculus , 2015, NeuroImage.

[14]  D H Hubel,et al.  Effects of varying stimulus size and color on single lateral geniculate cells in Rhesus monkeys. , 1966, Proceedings of the National Academy of Sciences of the United States of America.

[15]  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.

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

[17]  John H. R. Maunsell,et al.  Physiological correlates of perceptual learning in monkey V1 and V2. , 2002, Journal of neurophysiology.

[18]  Mark F. Bear,et al.  How Monocular Deprivation Shifts Ocular Dominance in Visual Cortex of Young Mice , 2004, Neuron.

[19]  Essa Yacoub,et al.  Functional mapping of the magnocellular and parvocellular subdivisions of human LGN , 2014, NeuroImage.

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

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

[22]  D. Purves,et al.  Correlated Size Variations in Human Visual Cortex, Lateral Geniculate Nucleus, and Optic Tract , 1997, The Journal of Neuroscience.

[23]  R. Vogels,et al.  Practicing Coarse Orientation Discrimination Improves Orientation Signals in Macaque Cortical Area V4 , 2011, Current Biology.

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

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

[26]  Yuka Sasaki,et al.  Different Dynamics of Performance and Brain Activation in the Time Course of Perceptual Learning , 2008, Neuron.

[27]  Takeo Watanabe,et al.  Neuroimaging Evidence for 2 Types of Plasticity in Association with Visual Perceptual Learning , 2016, Cerebral cortex.

[28]  D. Sagi Perceptual learning in Vision Research , 2011, Vision Research.

[29]  Keiji Tanaka,et al.  Human Ocular Dominance Columns as Revealed by High-Field Functional Magnetic Resonance Imaging , 2001, Neuron.

[30]  M. Bear,et al.  Molecular mechanism for loss of visual cortical responsiveness following brief monocular deprivation , 2003, Nature Neuroscience.

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

[32]  S Murray Sherman,et al.  Thalamus plays a central role in ongoing cortical functioning , 2016, Nature Neuroscience.

[33]  G. Blasdel,et al.  Physiological organization of layer 4 in macaque striate cortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[34]  Y. Saalmann,et al.  Cognitive and Perceptual Functions of the Visual Thalamus , 2011, Neuron.

[35]  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.

[36]  P. Lennie,et al.  Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. , 1984, The Journal of physiology.

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

[38]  Peng Zhang,et al.  Selective reduction of fMRI responses to transient achromatic stimuli in the magnocellular layers of the LGN and the superficial layer of the SC of early glaucoma patients , 2016, Human brain mapping.

[39]  Taiyong Bi,et al.  Function and Structure of Human Left Fusiform Cortex Are Closely Associated with Perceptual Learning of Faces , 2014, Current Biology.

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

[41]  A. J. Parker,et al.  Contrast sensitivity and orientation selectivity in lamina IV of the striate cortex of Old World monkeys , 1984, Experimental Brain Research.