Population receptive field and connectivity properties of the early visual cortex in human albinism

In albinism, the pathological decussation of the temporal retinal afferents at the optic chiasm leads to superimposed representations of opposing hemifields in the visual cortex. Here, we assessed the equivalence of the two representations and the cortico-cortical connectivity of the early visual areas. Applying fMRI-based population receptive field (pRF)-mapping (both hemifield and bilateral mapping) and connective field (CF)-modeling, we investigated the early visual cortex in 6 albinotic participants and 4 controls. In albinism, superimposed retinotopic representations of the contra- and ipsilateral visual hemifield were observed on the hemisphere contralateral to the stimulated eye. This was confirmed by the observation of bilateral pRFs during bilateral mapping. Hemifield mapping revealed similar pRF-sizes for both hemifield representations throughout V1 to V3. The typical increase of V1-sampling extent for V3 compared to V2 was not found for the albinotic participants. The similarity of the pRF-sizes for opposing visual hemifield representations highlights the equivalence of the two maps in the early visual cortex. The altered V1-sampling extent in V3 indicates the adaptation of cortico-cortical connections to the abnormal input of the visual cortex. These findings thus suggest that conservative developmental mechanisms are complemented by alterations of the extrastriate cortico-cortical connectivity. Highlights pRF mapping confirms cortical overlay of opposing visual hemifields in albinism. Equivalent information processing of both hemifields is indicated by similar pRF sizes. CF modeling indicates changes to the cortico-cortical connections at the level of V3.

[1]  D. Hubel,et al.  Receptive fields and functional architecture of monkey striate cortex , 1968, The Journal of physiology.

[2]  D. Creel Visual System Anomaly associated with Albinism in the Cat , 1971, Nature.

[3]  R. Guillery,et al.  Abnormal visual pathways in the brain of a human albino , 1975, Brain Research.

[4]  S. Holm A Simple Sequentially Rejective Multiple Test Procedure , 1979 .

[5]  H. Spekreijse,et al.  Evoked potentials in albinos: efficacy of pattern stimuli in detecting misrouted optic fibers. , 1981, Electroencephalography and clinical neurophysiology.

[6]  H Spekreijse,et al.  A decisive electrophysiological test for human albinism. , 1983, Electroencephalography and clinical neurophysiology.

[7]  John H. R. Maunsell,et al.  The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  R W Guillery,et al.  Abnormal central visual pathways in the brain of an albino green monkey (Cercopithecus aethiops) , 1984, The Journal of comparative neurology.

[9]  R. W. Guillery,et al.  Neural abnormalities of albinos , 1986, Trends in Neurosciences.

[10]  D. J. Felleman,et al.  Receptive field properties of neurons in area V3 of macaque monkey extrastriate cortex. , 1987, Journal of neurophysiology.

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

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

[13]  R. Turner,et al.  Event-Related fMRI: Characterizing Differential Responses , 1998, NeuroImage.

[14]  A. Dale,et al.  The representation of the ipsilateral visual field in human cerebral cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[15]  B. Wandell,et al.  Visualization and Measurement of the Cortical Surface , 2000, Journal of Cognitive Neuroscience.

[16]  Michael B Hoffmann,et al.  Organization of the Visual Cortex in Human Albinism , 2003, The Journal of Neuroscience.

[17]  G. Grön,et al.  Monocular visual activation patterns in albinism as revealed by functional magnetic resonance imaging , 2004, Human brain mapping.

[18]  Birgit Lorenz,et al.  Misrouting of the optic nerves in albinism: estimation of the extent with visual evoked potentials. , 2005, Investigative ophthalmology & visual science.

[19]  Takahiro Doi,et al.  Disparity-tuning characteristics of neuronal responses to dynamic random-dot stereograms in macaque visual area V4. , 2005, Journal of neurophysiology.

[20]  Michael B Hoffmann,et al.  Pigmentation predicts the shift in the line of decussation in humans with albinism , 2007, The European journal of neuroscience.

[21]  Michael B Hoffmann,et al.  Perceptual relevance of abnormal visual field representations: static visual field perimetry in human albinism , 2007, British Journal of Ophthalmology.

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

[23]  Michael B Hoffmann,et al.  Identifying human albinism: a comparison of VEP and fMRI. , 2008, Investigative ophthalmology & visual science.

[24]  M. Hoffmann,et al.  Self-organisation in the human visual system—Visuo-motor processing with congenitally abnormal V1 input , 2010, Neuropsychologia.

[25]  S. Dumoulin,et al.  The Relationship between Cortical Magnification Factor and Population Receptive Field Size in Human Visual Cortex: Constancies in Cortical Architecture , 2011, The Journal of Neuroscience.

[26]  P. Sinha,et al.  Superimposed Hemifields in Primary Visual Cortex of Achiasmic Individuals , 2012, Neuron.

[27]  Brian A. Wandell,et al.  Plasticity and Stability of the Visual System in Human Achiasma , 2012, Neuron.

[28]  Christopher D. Chambers,et al.  Cortical plasticity in the face of congenitally altered input into V1 , 2012, Cortex.

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

[30]  Jonathan Winawer,et al.  Connective field modeling , 2013, NeuroImage.

[31]  Gordon E Legge,et al.  Higher-contrast requirements for recognizing low-pass-filtered letters. , 2013, Journal of vision.

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

[33]  Koen V. Haak,et al.  Cortical connective field estimates from resting state fMRI activity , 2014, Front. Neurosci..

[34]  Oliver Speck,et al.  Impact of chiasma opticum malformations on the organization of the human ventral visual cortex , 2014, Human brain mapping.

[35]  H. Thieme,et al.  Visual Pathways in Humans With Ephrin-B1 Deficiency Associated With the Cranio-Fronto-Nasal Syndrome. , 2015, Investigative ophthalmology & visual science.

[36]  Serge O. Dumoulin,et al.  Congenital visual pathway abnormalities: a window onto cortical stability and plasticity , 2015, Trends in Neurosciences.

[37]  Nikos K. Logothetis,et al.  Nonlinear population receptive field changes in human area V5/MT+ of healthy subjects with simulated visual field scotomas , 2015, NeuroImage.

[38]  Alessio Fracasso,et al.  Bilateral population receptive fields in congenital hemihydranencephaly , 2016, Ophthalmic & physiological optics : the journal of the British College of Ophthalmic Opticians.

[39]  Kristine Krug,et al.  Neural architectures for stereo vision , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[40]  M. B. Hoffmann,et al.  Potenzial von fMRT für die Funktionsüberprüfung des pathologischen Sehsystems , 2017, Klinische Monatsblätter für Augenheilkunde.

[41]  M. Hoffmann,et al.  Interocular transfer of visual memory – Influence of visual impairment and abnormalities of the optic chiasm , 2019, Neuropsychologia.

[42]  Alessio Fracasso,et al.  Altered organization of the visual cortex in FHONDA syndrome , 2019, NeuroImage.