Visual motion integration by neurons in the middle temporal area of a New World monkey, the marmoset

Non‐technical summary  The machinery of motion vision is highly conserved across New World and Old World monkeys, according to our study of the marmoset visual cortex. The marmoset is a New World primate, part of a lineage that diverged from Old World monkeys some 30–40 million years ago. A small part of the cerebral cortex, area MT, can be identified anatomically in both New and Old World primates. In the macaque, an Old World primate, this area is thought to be important in analysing the motion of complex patterns. Here we quantified the capacity of neurons in area MT of marmosets to extract motion from complex patterns. We find the responses of neurons in area MT of marmosets to be indistinguishable from those in macaques, suggesting that the functional role of this small area of the visual cortex is highly conserved over evolution.

[1]  Christopher C. Pack,et al.  The role of V1 surround suppression in MT motion integration. , 2010, Journal of neurophysiology.

[2]  P. H. Schiller,et al.  Spatial frequency and orientation tuning dynamics in area V1 , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Chris Tailby,et al.  Adaptable Mechanisms That Regulate the Contrast Response of Neurons in the Primate Lateral Geniculate Nucleus , 2009, The Journal of Neuroscience.

[4]  C. Russo,et al.  Timing the origin of New World monkeys. , 2003, Molecular biology and evolution.

[5]  Chris J. Tinsley,et al.  The nature of V1 neural responses to 2D moving patterns depends on receptive-field structure in the marmoset monkey. , 2003, Journal of neurophysiology.

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

[7]  R Gattass,et al.  Cortical afferents of visual area MT in the Cebus monkey: Possible homologies between New and old World monkeys , 1993, Visual Neuroscience.

[8]  C. Gross,et al.  Visual topography of striate projection zone (MT) in posterior superior temporal sulcus of the macaque. , 1981, Journal of neurophysiology.

[9]  David R. Badcock,et al.  Two-stage analysis of the motion of 2-dimensional patterns, what is the first stage? , 1992, Vision Research.

[10]  T. Albright Direction and orientation selectivity of neurons in visual area MT of the macaque. , 1984, Journal of neurophysiology.

[11]  Alexander Thiele,et al.  Speed skills: measuring the visual speed analyzing properties of primate MT neurons , 2001, Nature Neuroscience.

[12]  J. Kaas,et al.  A representation of the visual field in the caudal third of the middle tempral gyrus of the owl monkey (Aotus trivirgatus). , 1971, Brain research.

[13]  John H. R. Maunsell,et al.  The middle temporal visual area in the macaque: Myeloarchitecture, connections, functional properties and topographic organization , 1981, The Journal of comparative neurology.

[14]  Eero P. Simoncelli,et al.  A model of neuronal responses in visual area MT , 1998, Vision Research.

[15]  J. Kaas,et al.  Retinotopic patterns of connections of area 17 with visual areas V‐II and MT in macaque monkeys , 1983, The Journal of comparative neurology.

[16]  S. Zeki,et al.  Response properties and receptive fields of cells in an anatomically defined region of the superior temporal sulcus in the monkey. , 1971, Brain research.

[17]  J. Movshon,et al.  Linearity and Normalization in Simple Cells of the Macaque Primary Visual Cortex , 1997, The Journal of Neuroscience.

[18]  G. Elston,et al.  Visuotopic organisation and neuronal response selectivity for direction of motion in visual areas of the caudal temporal lobe of the marmoset monkey (Callithrix jacchus): Middle temporal area, middle temporal crescent, and surrounding cortex , 1998, The Journal of comparative neurology.

[19]  Anthony J. Movshon,et al.  Visual Response Properties of Striate Cortical Neurons Projecting to Area MT in Macaque Monkeys , 1996, The Journal of Neuroscience.

[20]  G. Glazko,et al.  Estimation of divergence times for major lineages of primate species. , 2003, Molecular biology and evolution.

[21]  Eero P. Simoncelli,et al.  How MT cells analyze the motion of visual patterns , 2006, Nature Neuroscience.

[22]  F. Gallyas Silver staining of myelin by means of physical development. , 1979, Neurological research.

[23]  K. Rockland,et al.  Bistratified distribution of terminal arbors of individual axons projecting from area V1 to middle temporal area (MT) in the macaque monkey , 1989, Visual Neuroscience.

[24]  Colin Blakemore,et al.  Pattern motion is present in V1 of awake but not anaesthetized monkeys , 2004, The European journal of neuroscience.

[25]  Christopher C. Pack,et al.  Dynamic properties of neurons in cortical area MT in alert and anaesthetized macaque monkeys , 2001, Nature.

[26]  J Allman,et al.  Direction- and Velocity-Specific Responses from beyond the Classical Receptive Field in the Middle Temporal Visual Area (MT) , 1985, Perception.

[27]  K. Tanaka,et al.  Analysis of local and wide-field movements in the superior temporal visual areas of the macaque monkey , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  W. Newsome,et al.  A selective impairment of motion perception following lesions of the middle temporal visual area (MT) , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  J. Movshon,et al.  Nature and interaction of signals from the receptive field center and surround in macaque V1 neurons. , 2002, Journal of neurophysiology.

[30]  P. Lennie,et al.  Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. , 1984, The Journal of physiology.

[31]  Steven C. Dakin,et al.  Local and global limitations on direction integration assessed using equivalent noise analysis , 2005, Vision Research.

[32]  Ricardo Gattass,et al.  Electrophysiological Imaging of Functional Architecture in the Cortical Middle Temporal Visual Area of Cebus apella Monkey , 2003, The Journal of Neuroscience.

[33]  Nicholas J. Priebe,et al.  The Neural Representation of Speed in Macaque Area MT/V5 , 2003, The Journal of Neuroscience.

[34]  J. Movshon,et al.  The analysis of visual motion: a comparison of neuronal and psychophysical performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  R A Andersen,et al.  The response of area MT and V1 neurons to transparent motion , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  John H. R. Maunsell,et al.  Coding of image contrast in central visual pathways of the macaque monkey , 1990, Vision Research.

[37]  K. Mardia Statistics of Directional Data , 1972 .

[38]  S. Petersen,et al.  Visual response properties of neurons in four extrastriate visual areas of the owl monkey (Aotus trivirgatus): a quantitative comparison of medial, dorsomedial, dorsolateral, and middle temporal areas. , 1981, Journal of neurophysiology.

[39]  J. Movshon,et al.  Dynamics of motion signaling by neurons in macaque area MT , 2005, Nature Neuroscience.

[40]  C. Enroth-Cugell,et al.  The contrast sensitivity of retinal ganglion cells of the cat , 1966, The Journal of physiology.

[41]  G. Drummond Reporting ethical matters in The Journal of Physiology: standards and advice , 2009, The Journal of physiology.

[42]  D. J. Felleman,et al.  Receptive-field properties of neurons in middle temporal visual area (MT) of owl monkeys. , 1984, Journal of neurophysiology.

[43]  D. Ringach,et al.  Dynamics of Spatial Frequency Tuning in Macaque V1 , 2002, The Journal of Neuroscience.

[44]  R. Shapley,et al.  Orientation Selectivity in Macaque V1: Diversity and Laminar Dependence , 2002, The Journal of Neuroscience.

[45]  D. Bradley,et al.  Structure and function of visual area MT. , 2005, Annual review of neuroscience.

[46]  E. Adelson,et al.  The analysis of moving visual patterns , 1985 .

[47]  Christopher C. Pack,et al.  Temporal dynamics of a neural solution to the aperture problem in visual area MT of macaque brain , 2001, Nature.

[48]  H. Wilson,et al.  A psychophysically motivated model for two-dimensional motion perception , 1992, Visual Neuroscience.

[49]  Hiroaki Okamoto,et al.  MT neurons in the macaque exhibited two types of bimodal direction tuning as predicted by a model for visual motion detection , 1999, Vision Research.

[50]  E H Adelson,et al.  Spatiotemporal energy models for the perception of motion. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[51]  Leo L. Lui,et al.  Spatial and temporal frequency selectivity of neurons in the middle temporal visual area of new world monkeys (Callithrix jacchus) , 2007, The European journal of neuroscience.

[52]  M. Rosa,et al.  Chemoarchitecture of the middle temporal visual area in the marmoset monkey (Callithrix jacchus): Laminar distribution of calcium‐binding proteins (calbindin, parvalbumin) and nonphosphorylated neurofilament , 2007, The Journal of comparative neurology.