Layer-specific response properties of the human lateral geniculate nucleus and superior colliculus

The human LGN and SC consist of distinct layers, but their layer-specific response properties remain poorly understood. In this fMRI study, we characterized visual response properties of the magnocellular (M) and parvocellular (P) layers of the human LGN, as well as at different depths in the SC. Results show that fMRI is capable of resolving layer-specific signals from the LGN and SC. Compared to the P layers of the LGN, the M layers preferred higher temporal frequency, lower spatial frequency stimuli, and their responses saturated at lower contrast. Furthermore, the M layers are colorblind while the P layers showed robust response to both chromatic and achromatic stimuli. Visual responses in the SC were strongest in the superficial voxels, which showed similar spatiotemporal and contrast response properties as the M layers of the LGN, but were sensitive to color and responded strongly to isoluminant color stimulus. Thus, the non-invasive fMRI measures show that the M and P layers of human LGN have similar response properties as that observed in non-human primates and the superficial layers of the human SC prefer transient inputs but are not colorblind.

[1]  D. Tolhurst,et al.  Psychophysical evidence for sustained and transient detectors in human vision , 1973, The Journal of physiology.

[2]  N. Logothetis,et al.  High-Resolution fMRI Reveals Laminar Differences in Neurovascular Coupling between Positive and Negative BOLD Responses , 2012, Neuron.

[3]  Paul D. Gamlin,et al.  The Smooth Monostratified Ganglion Cell: Evidence for Spatial Diversity in the Y-Cell Pathway to the Lateral Geniculate Nucleus and Superior Colliculus in the Macaque Monkey , 2008, The Journal of Neuroscience.

[4]  Tony Ro,et al.  Extrageniculate mediation of unconscious vision in transcranial magnetic stimulation-induced blindsight. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[5]  G. Legge Sustained and transient mechanisms in human vision: Temporal and spatial properties , 1978, Vision Research.

[6]  John H. R. Maunsell,et al.  How parallel are the primate visual pathways? , 1993, Annual review of neuroscience.

[7]  Karl J. Friston,et al.  Statistical parametric mapping , 2013 .

[8]  Keith A Schneider,et al.  Subcortical Mechanisms of Feature-Based Attention , 2011, The Journal of Neuroscience.

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

[10]  Laurent Itti,et al.  Color-Related Signals in the Primate Superior Colliculus , 2009, The Journal of Neuroscience.

[11]  Peng Zhang,et al.  Layer-specific fMRI signals in the human LGN – An investigation of magnocellular and parvocellular pathways in normal subjects and glaucoma patients , 2014 .

[12]  Joseph V. Hajnal,et al.  Identification and characterisation of midbrain nuclei using optimised functional magnetic resonance imaging , 2012, NeuroImage.

[13]  David Ress,et al.  Endogenous Attention Signals Evoked by Threshold Contrast Detection in Human Superior Colliculus , 2014, The Journal of Neuroscience.

[14]  Larissa McKetton,et al.  Discriminating the eye-specific layers of the human lateral geniculate nucleus using high-resolution fMRI , 2012 .

[15]  Ronald S. Harwerth,et al.  Psychophysical evidence for sustained and transient channels in the monkey visual system , 1980, Vision Research.

[16]  Sabine Kastner,et al.  Retinotopic organization and functional subdivisions of the human lateral geniculate nucleus and superior colliculus , 2004 .

[17]  Marlene C. Richter,et al.  Retinotopic Organization and Functional Subdivisions of the Human Lateral Geniculate Nucleus: A High-Resolution Functional Magnetic Resonance Imaging Study , 2004, The Journal of Neuroscience.

[18]  Sabine Kastner,et al.  Visual responses of the human superior colliculus: a high-resolution functional magnetic resonance imaging study. , 2005, Journal of neurophysiology.

[19]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[20]  A. Cowey,et al.  Blindsight in man and monkey. , 1997, Brain : a journal of neurology.

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

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

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

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

[25]  D. Hubel,et al.  Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. , 1966, Journal of neurophysiology.

[26]  P. Toutouzas,et al.  A Magnetic Resonance Imaging Study , 2003 .

[27]  David Ress,et al.  Topography of covert visual attention in human superior colliculus. , 2010, Journal of neurophysiology.