Mapping cone- and rod-induced retinal responsiveness in macaque retina by optical imaging.

PURPOSE To map the distribution of cone- or rod-induced retinal responsiveness by optical imaging from macaque retina. METHODS The light reflectance changes in the posterior retina after a flash stimulus in anesthetized rhesus monkeys were measured by a modified fundus camera system equipped with a charge-coupled device (CCD) camera. The response topography of the optical signals was obtained in either light- or dark-adapted conditions. RESULTS With infrared observation light, the whole posterior pole became darkened after the stimulus. The response topography in light-adapted conditions demonstrated a steep peak of darkening at the fovea, together with the gradual decrease of signal intensity away from the fovea toward the periphery. In dark-adapted conditions, the optical signal showed additional peaks along the circular region surrounding the macula at the eccentricity of the optic disc, together with the central peak at the fovea. A statistically significant positive correlation was obtained between the light reflectance changes in infrared observation light and the focal responses in multifocal electroretinogram (mfERG) at the corresponding retinal locations. CONCLUSIONS The response topography in the retina, obtained by optical imaging, was consistent with psychophysical cone or rod sensitivity in humans and anatomic cone or rod distribution in humans and macaques. The cone- or rod-induced retinal responsiveness within the posterior pole region was noninvasively recorded within a short recording time.

[1]  M A Bearse,et al.  Imaging localized retinal dysfunction with the multifocal electroretinogram. , 1996, Journal of the Optical Society of America. A, Optics, image science, and vision.

[2]  G. Ghose,et al.  Form processing modules in primate area V4. , 1997, Journal of neurophysiology.

[3]  R. Turner,et al.  Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[4]  L L SLOAN,et al.  Peripheral visual acuity with special reference to scotopic illumination. , 1947, American journal of ophthalmology.

[5]  David Williams,et al.  The arrangement of the three cone classes in the living human eye , 1999, Nature.

[6]  E. Newman Voltage-dependent calcium and potassium channels in retinal glial cells , 1985, Nature.

[7]  D M Snodderly,et al.  Comparison of fluorescein angiography with microvascular anatomy of macaque retinas. , 1995, Experimental eye research.

[8]  D. Ts'o,et al.  Cortical functional architecture and local coupling between neuronal activity and the microcirculation revealed by in vivo high-resolution optical imaging of intrinsic signals. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[9]  D. Tank,et al.  Brain magnetic resonance imaging with contrast dependent on blood oxygenation. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Erich E. Sutter,et al.  The field topography of ERG components in man—I. The photopic luminance response , 1992, Vision Research.

[11]  M. Raichle,et al.  Stimulus rate dependence of regional cerebral blood flow in human striate cortex, demonstrated by positron emission tomography. , 1984, Journal of neurophysiology.

[12]  T. Wiesel,et al.  Functional architecture of cortex revealed by optical imaging of intrinsic signals , 1986, Nature.

[13]  T. Eames THE VISUAL FIELDS , 1955 .

[14]  A. Toga,et al.  The temporal/spatial evolution of optical signals in human cortex. , 1995, Cerebral cortex.

[15]  E. Birch,et al.  The relationship between rod perimetric thresholds and full-field rod ERGs in retinitis pigmentosa. , 1987, Investigative ophthalmology & visual science.

[16]  Shing-Chung Ngan,et al.  Functional magnetic resonance imaging of the retina. , 2002, Investigative ophthalmology & visual science.

[17]  T. Berendschot,et al.  Slow optical changes in human photoreceptors induced by light. , 2000, Investigative ophthalmology & visual science.

[18]  J. Read,et al.  Determination of human cone pigment density difference spectra in spatially resolved regions of the fovea , 1983, Vision Research.

[19]  A. Hendrickson,et al.  Human photoreceptor topography , 1990, The Journal of comparative neurology.

[20]  Kenneth R. Alexander,et al.  Human macular pigment assessed by imaging fundus reflectometry , 1989, Vision Research.

[21]  H. Ripps,et al.  "Rapid regeneration" in the cat retina: a case for spreading depression , 1981, The Journal of general physiology.

[22]  Uma Maheswari Rajagopalan,et al.  Localization of activity-dependent changes in blood volume to submillimeter-scale functional domains in cat visual cortex. , 2005, Cerebral cortex.

[23]  A. Villringer,et al.  Non-invasive optical spectroscopy and imaging of human brain function , 1997, Trends in Neurosciences.

[24]  F. Sengpiel,et al.  Optical imaging of intrinsic signals: recent developments in the methodology and its applications , 2004, Journal of Neuroscience Methods.

[25]  Noemi Bitterman,et al.  Development of laser-induced retinal damage in the rabbit , 1999, Graefe's Archive for Clinical and Experimental Ophthalmology.

[26]  D. Fitzpatrick,et al.  Patterns of excitation and inhibition evoked by horizontal connections in visual cortex share a common relationship to orientation columns , 1995, Neuron.

[27]  H. Kadono,et al.  Novel functional imaging technique from brain surface with optical coherence tomography enabling visualization of depth resolved functional structure in vivo , 2003, Journal of Neuroscience Methods.

[28]  D. Ts'o,et al.  Visual topography in primate V2: multiple representation across functional stripes , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  C. Riva,et al.  Flicker-evoked responses of human optic nerve head blood flow: luminance versus chromatic modulation. , 2001, Investigative ophthalmology & visual science.

[30]  B. MacVicar,et al.  Imaging of synaptically evoked intrinsic optical signals in hippocampal slices , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  E. Pulos Changes in rod sensitivity through adulthood. , 1989, Investigative ophthalmology & visual science.

[32]  S A Burns,et al.  Foveal cone photopigment distribution: small alterations associated with macular pigment distribution. , 1998, Investigative ophthalmology & visual science.

[33]  J. Mollon,et al.  Microspectrophotometric demonstration of four classes of photoreceptor in an old world primate, Macaca fascicularis. , 1980, The Journal of physiology.

[34]  C K Dorey,et al.  In vivo fluorescence of the ocular fundus exhibits retinal pigment epithelium lipofuscin characteristics. , 1995, Investigative ophthalmology & visual science.

[35]  Y. Miyake,et al.  Asymmetry of focal ERG in human macular region. , 1989, Investigative ophthalmology & visual science.

[36]  D. Ts'o,et al.  Functional organization of primate visual cortex revealed by high resolution optical imaging. , 1990, Science.

[37]  D. J. Brown,et al.  Peripheral visual acuity. , 1966, Archives of ophthalmology.

[38]  A Grinvald,et al.  Optical imaging reveals the functional architecture of neurons processing shape and motion in owl monkey area MT , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[39]  Y. Yamane,et al.  Complex objects are represented in macaque inferotemporal cortex by the combination of feature columns , 2001, Nature Neuroscience.

[40]  J. Bowmaker,et al.  Visual pigments of rods and cones in a human retina. , 1980, The Journal of physiology.

[41]  D. V. van Essen,et al.  Retinotopic organization of human visual cortex mapped with positron- emission tomography , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  C. Gilbert,et al.  Long-range horizontal connections and their role in cortical reorganization revealed by optical recording of cat primary visual cortex , 1995, Nature.

[43]  G. Ojemann,et al.  Optical imaging of epileptiform and functional activity in human cerebral cortex , 1992, Nature.

[44]  G. Blasdel,et al.  Voltage-sensitive dyes reveal a modular organization in monkey striate cortex , 1986, Nature.

[45]  D. Attwell,et al.  Electrogenic glutamate uptake is a major current carrier in the membrane of axolotl retinal glial cells , 1987, Nature.

[46]  A. Hendrickson,et al.  Photoreceptor topography of the retina in the adult pigtail macaque (Macaca nemestrina) , 1989, The Journal of comparative neurology.

[47]  G. Taga,et al.  Brain imaging in awake infants by near-infrared optical topography , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[48]  A. Reichenbach,et al.  Morphometric parameters of Müller (glial) cells dependent on their topographic localization in the nonmyelinated part of the rabbit retina. A consideration of functional aspects of radial glia , 1986, Journal of neurocytology.

[49]  A. Elsner,et al.  Mapping cone photopigment optical density. , 1993, Journal of the Optical Society of America. A, Optics and image science.

[50]  Ravi S. Menon,et al.  Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[51]  A. Hendrickson,et al.  Distribution of cones in human and monkey retina: individual variability and radial asymmetry. , 1987, Science.

[52]  S. Ogawa Brain magnetic resonance imaging with contrast-dependent oxygenation , 1990 .