Nonlinear population receptive field changes in human area V5/MT+ of healthy subjects with simulated visual field scotomas

There is extensive controversy over whether the adult visual cortex is able to reorganize following visual field loss (scotoma) as a result of retinal or cortical lesions. Functional magnetic resonance imaging (fMRI) methods provide a useful tool to study the aggregate receptive field properties and assess the capacity of the human visual cortex to reorganize following injury. However, these methods are prone to biases near the boundaries of the scotoma. Retinotopic changes resembling reorganization have been observed in the early visual cortex of normal subjects when the visual stimulus is masked to simulate retinal or cortical scotomas. It is not known how the receptive fields of higher visual areas, like hV5/MT+, are affected by partial stimulus deprivation. We measured population receptive field (pRF) responses in human area V5/MT+ of 5 healthy participants under full stimulation and compared them with responses obtained from the same area while masking the left superior quadrant of the visual field (“artificial scotoma” or AS). We found that pRF estimations in area hV5/MT+ are nonlinearly affected by the AS. Specifically, pRF centers shift towards the AS, while the pRF amplitude increases and the pRF size decreases near the AS border. The observed pRF changes do not reflect reorganization but reveal important properties of normal visual processing under different test-stimulus conditions.

[1]  A. T. Smith,et al.  Estimating receptive field size from fMRI data in human striate and extrastriate visual cortex. , 2001, Cerebral cortex.

[2]  T. Nealey,et al.  Magnocellular and parvocellular contributions to responses in the middle temporal visual area (MT) of the macaque monkey , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  H. Komatsu,et al.  Perceptual filling-in at the scotoma following a monocular retinal lesion in the monkey , 1997, Visual Neuroscience.

[4]  Brian A. Wandell,et al.  Plasticity and stability of visual field maps in adult primary visual cortex , 2009, Nature Reviews Neuroscience.

[5]  Leslie G. Ungerleider,et al.  Perceptual filling-in: a parametric study , 1998, Vision Research.

[6]  T. Wiesel,et al.  Receptive field dynamics in adult primary visual cortex , 1992, Nature.

[7]  P A Salin,et al.  Response selectivity of neurons in area MT of the macaque monkey during reversible inactivation of area V1. , 1992, Journal of neurophysiology.

[8]  U. Eysel,et al.  Increased synaptic plasticity in the surround of visual cortex lesions in rats , 2001, Neuroreport.

[9]  Daniel D. Dilks,et al.  Reorganization of Visual Processing in Macular Degeneration Is Not Specific to the “Preferred Retinal Locus” , 2009, The Journal of Neuroscience.

[10]  C. N. Guy,et al.  Motion specific responses from a blind hemifield. , 1996, Brain : a journal of neurology.

[11]  R Desimone,et al.  Both striate cortex and superior colliculus contribute to visual properties of neurons in superior temporal polysensory area of macaque monkey. , 1986, Journal of neurophysiology.

[12]  J. Kaas,et al.  Rapid reorganization of cortical maps in adult cats following restricted deafferentation in retina , 1992, Vision Research.

[13]  F. Sengpiel,et al.  Reorganization of Visual Cortical Maps after Focal Ischemic Lesions , 2003, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[14]  Brian A. Wandell,et al.  Population receptive field estimates in human visual cortex , 2008, NeuroImage.

[15]  Antony B. Morland,et al.  Population Receptive Field Dynamics in Human Visual Cortex , 2012, PloS one.

[16]  U. Eysel,et al.  Neuronal dysfunction at the border of focal lesions in cat visual cortex , 1991, Neuroscience Letters.

[17]  G. Elston,et al.  Visual Responses of Neurons in the Middle Temporal Area of New World Monkeys after Lesions of Striate Cortex , 2000, The Journal of Neuroscience.

[18]  U. Eysel,et al.  Shift from phasic to tonic GABAergic transmission following laser-lesions in the rat visual cortex , 2012, Pflügers Archiv - European Journal of Physiology.

[19]  A. Morland,et al.  The Role of Spared Calcarine Cortex and Lateral Occipital Cortex in the Responses of Human Hemianopes to Visual Motion , 2004, Journal of Cognitive Neuroscience.

[20]  C. Gross,et al.  Afferent basis of visual response properties in area MT of the macaque. II. Effects of superior colliculus removal , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  R. Held,et al.  Residual Visual Function after Brain Wounds involving the Central Visual Pathways in Man , 1973, Nature.

[22]  Leslie G. Ungerleider,et al.  Increased Activity in Human Visual Cortex during Directed Attention in the Absence of Visual Stimulation , 1999, Neuron.

[23]  J. Kaas,et al.  Receptive-field properties of deafferentated visual cortical neurons after topographic map reorganization in adult cats , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  I. Ohzawa,et al.  Receptive field structure in the visual cortex: does selective stimulation induce plasticity? , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[25]  A. A. Skavenski,et al.  Recovery of visual responses in foveal V1 neurons following bilateral foveal lesions in adult monkey , 2004, Experimental Brain Research.

[26]  Ione Fine,et al.  Minimizing biases in estimating the reorganization of human visual areas with BOLD retinotopic mapping. , 2013, Journal of vision.

[27]  N. Kanwisher,et al.  Reorganization of Visual Processing in Macular Degeneration , 2005, The Journal of Neuroscience.

[28]  M G Rosa,et al.  Monocular focal retinal lesions induce short–term topographic plasticity in adult cat visual cortex , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[29]  Hans-Jochen Heinze,et al.  Analysis of pathways mediating preserved vision after striate cortex lesions , 2002, Annals of neurology.

[30]  T. Mittmann,et al.  Lesion‐induced changes in NMDA receptor subunit mRNA expression in rat visual cortex , 2000, Neuroreport.

[31]  J. Kaas,et al.  Reorganization of retinotopic cortical maps in adult mammals after lesions of the retina. , 1990, Science.

[32]  C. Gross,et al.  Afferent basis of visual response properties in area MT of the macaque. I. Effects of striate cortex removal , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[34]  M. Rosa,et al.  Visuotopic reorganization in the primary visual cortex of adult cats following monocular and binocular retinal lesions. , 1996, Cerebral cortex.

[35]  S Zeki,et al.  Conscious visual perception without V1. , 1993, Brain : a journal of neurology.

[36]  U. Eysel,et al.  Dynamics and specificity of cortical map reorganization after retinal lesions. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[37]  G. Leuba,et al.  Comparison of neuronal and glial numerical density in primary and secondary visual cortex of man , 2004, Experimental Brain Research.

[38]  Nikos K. Logothetis,et al.  A new method for estimating population receptive field topography in visual cortex , 2013, NeuroImage.

[39]  Koen V. Haak,et al.  Abnormal visual field maps in human cortex: A mini-review and a case report , 2014, Cortex.

[40]  J. Horton,et al.  Monocular Core Zones and Binocular Border Strips in Primate Striate Cortex Revealed by the Contrasting Effects of Enucleation, Eyelid Suture, and Retinal Laser Lesions on Cytochrome Oxidase Activity , 1998, The Journal of Neuroscience.

[41]  Taosheng Liu,et al.  Retinotopic mapping of the visual cortex using functional magnetic resonance imaging in a patient with central scotomas from atrophic macular degeneration. , 2004, Ophthalmology.

[42]  Geoffrey M. Ghose,et al.  Attention directed by expectations enhances receptive fields in cortical area MT , 2010, Vision Research.

[43]  Frans W Cornelissen,et al.  Large-scale remapping of visual cortex is absent in adult humans with macular degeneration , 2011, Nature Neuroscience.

[44]  Frank Tong,et al.  Filling-in of visual phantoms in the human brain , 2005, Nature Neuroscience.

[45]  David A. Leopold,et al.  Blindsight depends on the lateral geniculate nucleus , 2010, Nature.

[46]  U. Eysel,et al.  Increased receptive field size in the surround of chronic lesions in the adult cat visual cortex. , 1999, Cerebral cortex.

[47]  G. Orban,et al.  Reorganization in the visual cortex after retinal and cortical damage. , 1999, Restorative neurology and neuroscience.

[48]  U. Eysel,et al.  Changes in NMDA-receptor function in the first week following laser-induced lesions in rat visual cortex. , 2012, Cerebral cortex.

[49]  Georgios A Keliris,et al.  Population receptive field analysis of the primary visual cortex complements perimetry in patients with homonymous visual field defects , 2014, Proceedings of the National Academy of Sciences.

[50]  L Weiskrantz,et al.  Visual capacity in the hemianopic field following a restricted occipital ablation. , 1974, Brain : a journal of neurology.

[51]  B. Wandell,et al.  V1 projection zone signals in human macular degeneration depend on task, not stimulus. , 2008, Cerebral cortex.

[52]  Daniel D. Dilks,et al.  Human Adult Cortical Reorganization and Consequent Visual Distortion , 2007, The Journal of Neuroscience.

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

[54]  B. Wandell,et al.  Visual field maps, population receptive field sizes, and visual field coverage in the human MT+ complex. , 2009, Journal of neurophysiology.

[55]  D J Heeger,et al.  Robust multiresolution alignment of MRI brain volumes , 2000, Magnetic resonance in medicine.

[56]  Kevin P. Moloney,et al.  Reorganization of visual processing is related to eccentric viewing in patients with macular degeneration. , 2008, Restorative neurology and neuroscience.

[57]  Guy Marchal,et al.  Multimodality image registration by maximization of mutual information , 1997, IEEE Transactions on Medical Imaging.

[58]  Christopher Kennard,et al.  Visual activation of extra-striate cortex in the absence of V1 activation , 2010, Neuropsychologia.

[59]  Daniel D. Dilks,et al.  Reorganization of visual processing in macular degeneration: Replication and clues about the role of foveal loss , 2008, Vision Research.

[60]  U. Eysel,et al.  Changes in intracellular calcium transients and LTP in the surround of visual cortex lesions in rats , 2003, Brain Research.

[61]  N. Logothetis,et al.  Lack of long-term cortical reorganization after macaque retinal lesions , 2005, Nature.