The Foveal Confluence in Human Visual Cortex

The human visual system devotes a significant proportion of its resources to a very small part of the visual field, the fovea. Foveal vision is crucial for natural behavior and many tasks in daily life such as reading or fine motor control. Despite its significant size, this part of cortex is rarely investigated and the limited data have resulted in competing models of the layout of the foveal confluence in primate species. Specifically, how V2 and V3 converge at the central fovea is the subject of debate in primates and has remained “terra incognita” in humans. Using high-resolution fMRI (1.2 × 1.2 × 1.2 mm3) and carefully designed visual stimuli, we sought to accurately map the human foveal confluence and hence disambiguate the competing theories. We find that V1, V2, and V3 are separable right into the center of the foveal confluence, and V1 ends as a rounded wedge with an affine mapping of the foveal singularity. The adjacent V2 and, in contrast to current concepts from macaque monkey, also V3 maps form continuous bands (∼5 mm wide) around the tip of V1. This mapping results in a highly anisotropic representation of the visual field in these areas. Unexpectedly, for the centermost 0.75°, the cortical representations for both V2 and V3 are larger than that of V1, indicating that more neuronal processing power is dedicated to second-level analysis in this small but important part of the visual field.

[1]  S. Zeki Representation of central visual fields in prestriate cortex of monkey. , 1969, Brain research.

[2]  S. Klein,et al.  Vernier acuity, crowding and cortical magnification , 1985, Vision Research.

[3]  John H. R. Maunsell,et al.  The projections from striate cortex (V1) to areas V2 and V3 in the macaque monkey: Asymmetries, areal boundaries, and patchy connections , 1986, The Journal of comparative neurology.

[4]  W T Newsome,et al.  Ventral posterior visual area of the macaque: Visual topography and areal boundaries , 1986, The Journal of comparative neurology.

[5]  John H. R. Maunsell,et al.  Topographic organization of the middle temporal visual area in the macaque monkey: Representational biases and the relationship to callosal connections and myeloarchitectonic boundaries , 1987, The Journal of comparative neurology.

[6]  C. Gross,et al.  Visuotopic organization and extent of V3 and V4 of the macaque , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  I. Rentschler,et al.  Contrast thresholds for identification of numeric characters in direct and eccentric view , 1991, Perception & psychophysics.

[8]  D. Levi,et al.  The two-dimensional shape of spatial interaction zones in the parafovea , 1992, Vision Research.

[9]  Adrian T. Lee,et al.  fMRI of human visual cortex , 1994, Nature.

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

[11]  E. DeYoe,et al.  Mapping striate and extrastriate visual areas in human cerebral cortex. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[12]  R Gattass,et al.  Area V4 in Cebus monkey: extent and visuotopic organization. , 1998, Cerebral cortex.

[13]  P. Boesiger,et al.  SENSE: Sensitivity encoding for fast MRI , 1999, Magnetic resonance in medicine.

[14]  Ricardo Gattass,et al.  Third tier ventral extrastriate cortex in the New World monkey, Cebus apella , 2000, Experimental Brain Research.

[15]  M. Rosa,et al.  Visual areas in lateral and ventral extrastriate cortices of the marmoset monkey , 2000, The Journal of comparative neurology.

[16]  J. Kaas,et al.  Connectional and Architectonic Evidence for Dorsal and Ventral V3, and Dorsomedial Area in Marmoset Monkeys , 2001, The Journal of Neuroscience.

[17]  J. Kaas,et al.  Visual cortex organization in primates: theories of V3 and adjoining visual areas. , 2001, Progress in brain research.

[18]  R. Tootell,et al.  Where is 'dorsal V4' in human visual cortex? Retinotopic, topographic and functional evidence. , 2001, Cerebral cortex.

[19]  J. Kaas,et al.  Evidence for a Modified V3 with Dorsal and Ventral Halves in Macaque Monkeys , 2002, Neuron.

[20]  B. Fischer,et al.  Visual field representations and locations of visual areas V1/2/3 in human visual cortex. , 2003, Journal of vision.

[21]  J. Rovamo,et al.  Visual resolution, contrast sensitivity, and the cortical magnification factor , 2004, Experimental Brain Research.

[22]  R. Vautin,et al.  Magnification factor and receptive field size in foveal striate cortex of the monkey , 2004, Experimental Brain Research.

[23]  Nikos K Logothetis,et al.  On the nature of the BOLD fMRI contrast mechanism. , 2004, Magnetic resonance imaging.

[24]  Marcello G P Rosa,et al.  Brain maps, great and small: lessons from comparative studies of primate visual cortical organization , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[25]  Alex R. Wade,et al.  Extended Concepts of Occipital Retinotopy , 2005 .

[26]  R. Gattass,et al.  Cortical visual areas in monkeys: location, topography, connections, columns, plasticity and cortical dynamics , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[27]  D. Heeger,et al.  Two Retinotopic Visual Areas in Human Lateral Occipital Cortex , 2006, The Journal of Neuroscience.

[28]  Junjie Liu,et al.  Laminar profiles of functional activity in the human brain , 2007, NeuroImage.

[29]  B. Wandell,et al.  Visual Field Maps in Human Cortex , 2007, Neuron.

[30]  Kathleen A. Hansen,et al.  Topographic Organization in and near Human Visual Area V4 , 2007, The Journal of Neuroscience.

[31]  Alex R. Wade,et al.  Two-dimensional mapping of the central and parafoveal visual field to human visual cortex. , 2007, Journal of neurophysiology.

[32]  N. Kanwisher,et al.  Only some spatial patterns of fMRI response are read out in task performance , 2007, Nature Neuroscience.