Psychophysical measurement of marmoset acuity and myopia

The common marmoset has attracted increasing interest as a model for visual neuroscience. A measurement of fundamental importance to ensure the validity of visual studies is spatial acuity. The marmoset has excellent acuity that has been reported at the fovea to be nearly half that of the human (Ordy and Samorajski [ ]: Vision Res 8:1205–1225), a value that is consistent with them having similar photoreceptor densities combined with their smaller eye size (Troilo et al. [ ]: Vision Res 33:1301–1310). Of interest, the marmoset exhibits a higher proportion of cones than rods in peripheral vision than human or macaque, which in principle could endow them with better peripheral acuity depending on how those signals are pooled in subsequent processing. Here, we introduce a simple behavioral paradigm to measure acuity and then test how acuity in the marmoset scales with eccentricity. We trained subjects to fixate a central point and detect a peripheral Gabor by making a saccade to its location. First, we found that accurate assessment of acuity required correction for myopia in all adult subjects. This is an important point because marmosets raised in laboratory conditions often have mild to severe myopia (Graham and Judge [ ]: Vision Res 39:177–187), a finding that we confirm, and that would limit their utility for studies of vision if uncorrected. With corrected vision, we found that their acuity scales with eccentricity similar to that of humans and macaques, having roughly half the value of the human and with no clear departure for higher acuity in the periphery. © 2016 Wiley Periodicals, Inc. Develop Neurobiol 77: 300–313, 2017

[1]  D. W. Watkins,et al.  Grating visibility as a function of orientation and retinal eccentricity , 1975, Vision Research.

[2]  D. Newport,et al.  Transient natural convection in a conducting enclosure heated from above , 2013, J. Vis..

[3]  Michael S. Osmanski,et al.  The Role of Harmonic Resolvability in Pitch Perception in a Vocal Nonhuman Primate, the Common Marmoset (Callithrix jacchus) , 2013, The Journal of Neuroscience.

[4]  W. Kwan,et al.  The Early Maturation of Visual Cortical Area MT is Dependent on Input from the Retinorecipient Medial Portion of the Inferior Pulvinar , 2012, The Journal of Neuroscience.

[5]  C. Wildsoet,et al.  Form deprivation myopia in mature common marmosets (Callithrix jacchus). , 2000, Investigative ophthalmology & visual science.

[6]  W. Raub From the National Institutes of Health. , 1990, JAMA.

[7]  D. Troilo,et al.  The response to visual form deprivation differs with age in marmosets. , 2005, Investigative ophthalmology & visual science.

[8]  Earl L. Smith,et al.  Protective effects of high ambient lighting on the development of form-deprivation myopia in rhesus monkeys. , 2012, Investigative ophthalmology & visual science.

[9]  A Bradley,et al.  Effects of refractive error on detection acuity and resolution acuity in peripheral vision. , 1997, Investigative ophthalmology & visual science.

[10]  Xiaoqin Wang,et al.  Neural representations of temporally asymmetric stimuli in the auditory cortex of awake primates. , 2001, Journal of neurophysiology.

[11]  Andrew R Whatham,et al.  Compensatory changes in eye growth and refraction induced by daily wear of soft contact lenses in young marmosets , 2001, Vision Research.

[12]  B. Dreher,et al.  The visual pathways of eutherian mammals and marsupials develop according to a common timetable. , 1990, Brain, behavior and evolution.

[13]  C. Wildsoet,et al.  Choroidal thickness changes during altered eye growth and refractive state in a primate. , 2000, Investigative ophthalmology & visual science.

[14]  D. Troilo,et al.  Change in the synthesis rates of ocular retinoic acid and scleral glycosaminoglycan during experimentally altered eye growth in marmosets. , 2006, Investigative ophthalmology & visual science.

[15]  Jude F. Mitchell,et al.  Correction of refractive errors in rhesus macaques (Macaca mulatta) involved in visual research. , 2014, Comparative medicine.

[16]  David A. Leopold,et al.  The marmoset monkey as a model for visual neuroscience , 2015, Neuroscience Research.

[17]  A. Bradley,et al.  Characterization of spatial aliasing and contrast sensitivity in peripheral vision , 1996, Vision Research.

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

[19]  Lynne Kiorpes,et al.  Development of contour integration in macaque monkeys , 2003, Visual Neuroscience.

[20]  J. Maunsell,et al.  Psychophysical measurement of contrast sensitivity in the behaving mouse. , 2012, Journal of neurophysiology.

[21]  Tristan A. Chaplin,et al.  Representation of the visual field in the primary visual area of the marmoset monkey: Magnification factors, point‐image size, and proportionality to retinal ganglion cell density , 2013, The Journal of comparative neurology.

[22]  Paul R. Martin,et al.  Comparison of photoreceptor spatial density and ganglion cell morphology in the retina of human, macaque monkey, cat, and the marmoset Callithrix jacchus , 1996, The Journal of comparative neurology.

[23]  A. Cowey,et al.  The ganglion cell and cone distributions in the monkey's retina: Implications for central magnification factors , 1985, Vision Research.

[24]  D. Troilo,et al.  Decreased proteoglycan synthesis associated with form deprivation myopia in mature primate eyes. , 2000, Investigative ophthalmology & visual science.

[25]  John H. Reynolds,et al.  Active Vision in Marmosets: A Model System for Visual Neuroscience , 2014, The Journal of Neuroscience.

[26]  W. Merigan,et al.  Spatial resolution across the macaque retina , 1990, Vision Research.

[27]  A. Bradley,et al.  Neural bandwidth of veridical perception across the visual field , 2016, Journal of vision.

[28]  D. Williams,et al.  Cone spacing and the visual resolution limit. , 1987, Journal of the Optical Society of America. A, Optics and image science.

[29]  C. Wildsoet,et al.  Diurnal rhythms in intraocular pressure, axial length, and choroidal thickness in a primate model of eye growth, the common marmoset. , 2002, Investigative ophthalmology & visual science.

[30]  J. Ordy,et al.  Visual acuity and ERG-CFF in relation to the morphologic organization of the retina among diurnal and nocturnal primates. , 1968, Vision research.

[31]  B. B. Lee,et al.  Topography of ganglion cells and photoreceptors in the retina of a New World monkey: The marmoset Callithrix jacchus , 1996, Visual Neuroscience.

[32]  Denis G. Pelli,et al.  ECVP '07 Abstracts , 2007, Perception.

[33]  David A. Leopold,et al.  Marmosets: A Neuroscientific Model of Human Social Behavior , 2016, Neuron.

[34]  D. Troilo,et al.  Accommodation and induced myopia in marmosets , 2007, Vision Research.

[35]  D. Teller,et al.  Operant measurements of contrast sensitivity in infant macaque monkeys during normal development , 1988, Vision Research.

[36]  J. Movshon,et al.  Neural limitations on visual development in primates: Beyond striate cortex , 2014 .

[37]  Evan D. Remington,et al.  An Operant Conditioning Method for Studying Auditory Behaviors in Marmoset Monkeys , 2012, PloS one.

[38]  D. Teller,et al.  Development of contrast sensitivity in infant Macaca nemestrina monkeys. , 1980, Science.

[39]  David Troilo,et al.  Visual optics and retinal cone topography in the common marmoset (Callithrix jacchus) , 1993, Vision Research.

[40]  Lynne Kiorpes,et al.  Visual development in primates: Neural mechanisms and critical periods , 2015, Developmental neurobiology.

[41]  The Visual Pathways of Eutherian Mammals and Marsupials Develop According to a Common Timetable (Part 2 of 2) , 1990 .

[42]  J. Movshon,et al.  Analysis of the development of spatial contrast sensitivity in monkey and human infants. , 1988, Journal of the Optical Society of America. A, Optics and image science.

[43]  S. Judge,et al.  Ocular development and visual deprivation myopia in the common marmoset (Callithrix jacchus) , 1993, Vision Research.

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

[45]  D. M. Pessoa,et al.  Effect of luminosity on color discrimination of dichromatic marmosets (Callithrix jacchus). , 2012, Journal of the Optical Society of America. A, Optics, image science, and vision.

[46]  Ann Nour,et al.  Visual Psychophysics and Physiological Optics The Effect of Simultaneous Negative and Positive Defocus on Eye Growth and Development of Refractive State in Marmosets , 2012 .