Clustering of response selectivity in the medial superior temporal area of extrastriate cortex in the macaque monkey

Ever since being described by Mountcastle (Mountcastle, 1957), columnar organization of sensory cortical areas has provided key leverage into understanding the functional organization of neocortex. Columnar or clustered organization of neurons sharing like properties is now known to be widespread, and probably universal in primary sensory areas. Visual cortex in primates consists of a primary area and a large number of secondary areas, which are organized in a manner both hierarchical and parallel (Felleman & Van Essen, 1991; Young, 1993; Young et al., 1995). One major component in the organization of extrastriate visual cortex appears to be the division into dorsal and ventral "streams" of processing (Ungerleider & Mishkin, 1982), each of which is organized hierarchically. Within each, columnar organization exists at early stages, but becomes less clear at higher levels. Columnar organization has been described at the highest level of the ventral stream, inferotemporal cortex (IT, Saleem et al., 1993; Fujita & Fujita, 1996; Tanaka, 1996), but has not been well characterized at the higher levels of the dorsal stream. Hints of such organization are found in the literature (Saito et al., 1986; Lagae et al., 1994), but systematic measurements are needed. In this paper, I report the existence of clustered organization in the medial superior temporal area (MST) of the dorsal stream, which is arguably the highest dominantly visual area on this pathway. I have measured the selectivity of both single- and multiple-unit activity along oblique electrode penetrations through this area to three different kinds of optic flow stimuli, and find that nearby neurons are more similar in their tuning than are more distant ones. This observation documents the existence of some form of clustered organization and supports the importance of this area in the processing of optic flow information.

[1]  V. Mountcastle Modality and topographic properties of single neurons of cat's somatic sensory cortex. , 1957, Journal of neurophysiology.

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

[3]  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.

[4]  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.

[5]  S. Zeki Functional organization of a visual area in the posterior bank of the superior temporal sulcus of the rhesus monkey , 1974, The Journal of physiology.

[6]  B. Richmond,et al.  Implantation of magnetic search coils for measurement of eye position: An improved method , 1980, Vision Research.

[7]  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.

[8]  Leslie G. Ungerleider Two cortical visual systems , 1982 .

[9]  Lance M. Optican,et al.  Unix-based multiple-process system, for real-time data acquisition and control , 1982 .

[10]  D C Van Essen,et al.  Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. , 1983, Journal of neurophysiology.

[11]  R. Desimone,et al.  Columnar organization of directionally selective cells in visual area MT of the macaque. , 1984, Journal of neurophysiology.

[12]  D. Hubel,et al.  Anatomy and physiology of a color system in the primate visual cortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  Keiji Tanaka,et al.  Integration of direction signals of image motion in the superior temporal sulcus of the macaque monkey , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  Leslie G. Ungerleider,et al.  Cortical connections of visual area MT in the macaque , 1986, The Journal of comparative neurology.

[15]  田中 啓治 Analysis of Local and Wide-Field Movements in the Superior Temporal Visual Areas of the Macaque Monkey , 1987 .

[16]  Hidehiko Komatsu,et al.  A grid system and a microsyringe for single cell recording , 1988, Journal of Neuroscience Methods.

[17]  H. Komatsu,et al.  Relation of cortical areas MT and MST to pursuit eye movements. I. Localization and visual properties of neurons. , 1988, Journal of neurophysiology.

[18]  Daniel J. Hannon,et al.  Direction of self-motion is perceived from optical flow , 1988, Nature.

[19]  K. Tanaka,et al.  Underlying mechanisms of the response specificity of expansion/contraction and rotation cells in the dorsal part of the medial superior temporal area of the macaque monkey. , 1989, Journal of neurophysiology.

[20]  K. Tanaka,et al.  Analysis of motion of the visual field by direction, expansion/contraction, and rotation cells clustered in the dorsal part of the medial superior temporal area of the macaque monkey. , 1989, Journal of neurophysiology.

[21]  R. Wurtz,et al.  Sensitivity of MST neurons to optic flow stimuli. I. A continuum of response selectivity to large-field stimuli. , 1991, Journal of neurophysiology.

[22]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[23]  James A. Crowell,et al.  The perception of heading during eye movements , 1992, Nature.

[24]  K. Rockland,et al.  Specific and columnar projection from area TEO to TE in the macaque inferotemporal cortex. , 1993, Cerebral cortex.

[25]  M. Young The organization of neural systems in the primate cerebral cortex , 1993, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[26]  R. Born,et al.  Segregation of global and local motion processing in primate middle temporal visual area , 1993, Nature.

[27]  G. Orban,et al.  Responses of macaque STS neurons to optic flow components: a comparison of areas MT and MST. , 1994, Journal of neurophysiology.

[28]  W. Newsome,et al.  Neuronal and psychophysical sensitivity to motion signals in extrastriate area MST of the macaque monkey , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  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.

[30]  M P Young,et al.  Non-metric multidimensional scaling in the analysis of neuroanatomical connection data and the organization of the primate cortical visual system. , 1995, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[31]  R. Wurtz,et al.  Response of monkey MST neurons to optic flow stimuli with shifted centers of motion , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  I Fujita,et al.  Intrinsic connections in the macaque inferior temporal cortex , 1996, The Journal of comparative neurology.

[33]  R. Andersen,et al.  Mechanisms of Heading Perception in Primate Visual Cortex , 1996, Science.

[34]  Keiji Tanaka,et al.  Inferotemporal cortex and object vision. , 1996, Annual review of neuroscience.

[35]  R. Wurtz,et al.  Medial Superior Temporal Area Neurons Respond to Speed Patterns in Optic Flow , 1997, The Journal of Neuroscience.