Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-24T06:51:08.308Z Has data issue: false hasContentIssue false
  • English
  • Français

Radial motion bias in macaque frontal eye field

Published online by Cambridge University Press:  09 March 2006

QUAN XIAO ,
ANDREI BARBORICA  and
VINCENT P. FERRERA
QUAN XIAO
Affiliation:
Columbia University, Department of Psychiatry, Center for Neurobiology and Behavior, David Mahoney Center for Brain and Behavior Research, New York, New York
ANDREI BARBORICA
Affiliation:
Columbia University, Department of Psychiatry, Center for Neurobiology and Behavior, David Mahoney Center for Brain and Behavior Research, New York, New York
VINCENT P. FERRERA
Affiliation:
Columbia University, Department of Psychiatry, Center for Neurobiology and Behavior, David Mahoney Center for Brain and Behavior Research, New York, New York
Get access Rights & Permissions [Opens in a new window]

Abstract

The visual responsiveness and spatial tuning of frontal eye field (FEF) neurons were determined using a delayed memory saccade task. Neurons with visual responses were then tested for direction selectivity using moving random dot patterns centered in the visual receptive field. The preferred axis of motion showed a significant tendency to be aligned with the receptive-field location so as to favor motion toward or away from the center of gaze. Centrifugal (outward) motion was preferred over centripetal motion. Motion-sensitive neurons in FEF thus appear to have a direction bias at the population level. This bias may facilitate the detection or discrimination of expanding optic flow patterns. The direction bias is similar to that seen in visual area MT and in posterior parietal cortex, from which FEF receives afferent projections. The outward motion bias may explain asymmetries in saccades made to moving targets. A representation of optic flow in FEF might be useful for planning eye movements during navigation.

Keywords

MonkeyFrontal eye fieldOptic flow
Type
Research Article
Information
Visual Neuroscience , Volume 23 , Issue 1 , January 2006 , pp. 49 - 60
Copyright
2006 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Albright, T.D. (1989). Centrifugal directional bias in the middle temporal visual area (MT) of the macaque. Visual Neuroscience 2(2), 177–188.Google Scholar
Anderson, K.C. & Siegel, R.M. (1999). Optic flow selectivity in the anterior superior temporal polysensory area, STPa, of the behaving monkey. Journal of Neuroscience 19(7), 2681–2692.Google Scholar
Barbas, H. & Mesulam, M.M. (1981). Organization of afferent input to subdivisions of area 8 in the rhesus monkey. Journal of Comparative Neurology 200(3), 407–431.Google Scholar
Barborica, A. & Ferrera, V.P. (2003). Estimating invisible target speed from neuronal activity in monkey frontal eye field. Nature Neuroscience 6(1), 66–74.Google Scholar
Bauer, R. & Dow, B.M. (1989). Complementary global maps for orientation coding in upper and lower layers of the monkey foveal striate cortex. Experimental Brain Research 76, 503–509.Google Scholar
Bauer, R., Dow, B.M., Synder, A.Z., & Vautin, R.G. (1983). Orientation shift between upper and lower layers in monkey visual cortex. Experimental Brain Research 50, 133–145.Google Scholar
Britten, C.M. & Van Wezel, R.J. (2002). Area MST and heading perception in macaque monkeys. Cerebral Cortex 12(7), 692–701.Google Scholar
Bruce, C.J. & Goldberg, M.E. (1985). Primate frontal eye fields. I. Single neurons discharging before saccades. Journal of Neurophysiology 53, 603–635.Google Scholar
Bruce, C.J., Goldberg, M.E., Bushnell, M.C., & Stanton, G.B. (1985). Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked eye movements. Journal of Neurophysiology 53, 714–734.Google Scholar
Busettini, C., Masson, G.S., & Miles, F.A. (1997). Radial optic flow induces vergence eye movements with ultra-short latencies. Nature 390, 512–515.Google Scholar
Clifford, C.W.G., Beardsley, S.A., & Vaina, L.M. (1999). The perception and discrimination of speed in complex motion. Vision Research 39, 2213–2227.Google Scholar
Duffy, C.J. (2000). Optic flow analysis for self-movement perception. International Review of Neurobiology 44, 199–218.Google Scholar
Dukelow, S.P., DeSouza, J.F., Culham, J.C., van den Berg, A.V., Menon, R.S., & Vilis, T. (2001). Distinguishing subregions of the human MT+ complex using visual fields and pursuit eye movements. Journal of Neurophysiology 86(4), 1991–2000.Google Scholar
Ferraina, S., Pare, M., & Wurtz, R.H. (2000). Disparity sensitivity of frontal eye field neurons. Journal of Neurophysiology 83(1), 625–629.Google Scholar
Fukushima, K., Yamanobe, T., Shinmei, Y., Fukushima, J., Kurkin, S., & Peterson, B.W. (2002). Coding of smooth eye movements in three-dimensional space by frontal cortex. Nature 419, 157–162.Google Scholar
Funahashi, S., Bruce, C.J., & Goldman-Rakic, P.S. (1989). Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. Journal of Neurophysiology 61, 331–349.Google Scholar
Gamlin, P.D. & Yoon, K. (2000). An area for vergence eye movement in primate frontal cortex. Nature 407, 1003–1007.Google Scholar
Gibson, J.J. (1950). The Perception of the Visual World. Boston, Massachusetts: Hougton Mifflin.
Gottlieb, J.P., Bruce, C.J., & MacAvoy, M.G. (1993). Smooth eye movements elicited by microstimulation in the primate frontal eye field. Journal of Neurophysiology 69(3), 786–799.Google Scholar
Gottlieb, J.P., MacAvoy, M.G., & Bruce, C.J. (1994). Neural responses related to smooth-pursuit eye movements and their correspondence with electrically elicited smooth eye movements in the primate frontal eye field. Journal of Neurophysiology 72(4), 1634–1653.Google Scholar
Graziano, M.S., Andersen, R.A., & Snowden, R.J. (1994). Tuning of MST neurons to spiral motions. Journal of Neuroscience 14(1), 54–67.Google Scholar
Greenlee, M.W. (2000). Human cortical areas underlying the perception of optic flow: brain imaging studies. International Review of Neurobiology 44, 269–292.Google Scholar
Horwitz, G.D. & Newsome, W.T. (2001). Target selection for saccadic eye movements: Direction-selective visual responses in the superior colliculus. Journal of Neurophysiology 86, 2527–2542.Google Scholar
Inoue, Y., Takemura, A., Suehiro, K., Kodaka, Y., & Kawano, K. (1998). Short-latency vergence eye movements elicited by looming step in monkeys. Neuroscience Research 32(2), 185–188.Google Scholar
Judge, S.J., Richmond, B.J., & Chu, F.C. (1980). Implantation of magnetic search coils for measurement of eye position: An improved method. Vision Research 20, 535–538.Google Scholar
Kim, J.N. & Shadlen, M.N. (1999). Neural correlates of a decision in the dorsolateral prefrontal cortex of the macaque. Nature Neuroscience 2(2), 176–185.Google Scholar
Koenderink, J.J. (1986). Optic flow. Vision Research 26, 161–180.Google Scholar
Land, M.F. & Lee, D.N. (1994). Where we look when we steer. Nature 369(6483), 742–744.Google Scholar
Lappe, M. & Hoffmann, K.-P. (2000). Optic flow and eye movements. In Neuronal Processing of Optic Flow, ed. Lappe, M., Academic Press. International Review of Neurobiology 44, 29–47.Google Scholar
Lappe, M., Pekel, M., & Hoffmann, K.-P. (1998). Optokinetic eye movements elicited by radial optic flow in the macaque monkey. Journal of Neurophysiology 79, 1461–1480.Google Scholar
Lappe, M. & Rauschecker, J.P. (1994). Heading detection from optic flow. Nature 369, 712–713.Google Scholar
Leventhal, A.G. (1983). Relationship between preferred orientation and receptive field position of neurons in cat striate cortex. Journal of Comparative Neurology 220, 476–483.Google Scholar
Li, B., Li, B.W., Chen, Y., Wang, L.H., & Diao, Y.C. (2000). Response properties of PMLS and PLLS neurons to simulated optic flow patterns. European Journal of Neuroscience 12(5), 1534–1544.Google Scholar
Longuet-Higgins, H.C. & Prazdny, K. (1980). The interpretation of a moving retinal image. Proceedings of the Royal Society B (London) 208(1173), 385–397.Google Scholar
MacAvoy, M.G., Gottlieb, J.P., & Bruce, C.J. (1991). Smooth-pursuit eye movement representation in the primate frontal eye field. Cerebral Cortex 1(1), 95–102.Google Scholar
Merchant, H., Battaglia-Mayer, A., & Georgopoulos, A.P. (2001). Effects of optic flow in motor cortex and area 7a. Journal of Neurophysiology 86(4), 1937–1954.Google Scholar
Merchant, H., Battaglia-Mayer, A., & Georgopoulos, A.P. (2003). Functional organization of parietal neuronal responses to optic-flow stimuli. Journal of Neurophysiology 90(2), 675–682.Google Scholar
Morrone, M.C., Burr, D.C., DiPietro, S., & Stefanelli, M.-A. (1999). Cardinal directions for visual optic flow. Current Biology 9, 763–766.Google Scholar
Morrone, M.C., Tosetti, M., Montanaro, D., Fiorentini, A., Cioni, G., & Burr, D.C. (2000). A cortical area that responds specifically to optic flow, revealed by fMRI. Nature Neuroscience 3(12), 1322–1328.Google Scholar
Opris, I., Barborica, A., & Ferrera, V.P. (2001). On the gap effect for saccades evoked by electrical microstimulation of frontal eye fields in monkeys. Experimental Brain Research 138, 1–7.Google Scholar
Peuskens, H., Sunaert, S., Dupont, P., Van Hecke, P., & Orban, G.A. (2001). Human brain regions involved in heading estimation. Journal of Neuroscience 21(7), 2451–2461.Google Scholar
Priebe, N.J. & Lisberger, S.G. (2004). Estimating target speed from the population response in visual area MT. Journal of Neuroscience 24(8), 1907–1916.Google Scholar
Priebe, N.J., Cassanello, C.R., & Lisberger, S.G. (2003). The neural representation of speed in macaque area MT/V5. Journal of Neuroscience 23(13), 5650–5661.Google Scholar
Paxinos, G., Huang, X.F., & Toga, A.W. (2000). The Rhesus Monkey Brain in Stereotaxic Coordinates. San Diego, CA: Academic Press.
Perrone, J.A. (1992). Model for the computation of self-motion in biological systems. Journal of the Optical Society of America A 9, 177–194.Google Scholar
Perrone, J.A. & Stone, L.S. (1994). A model of self-motion estimation within primate extrastriate visual cortex. Vision Research 34, 2917–2938.Google Scholar
Raffi, M., Squatrito, S., & Maioli, M.G. (2002). Neuronal responses to optic flow in monkey parietal area PEc. Cerebral Cortex 12, 639–646.Google Scholar
Rauschecker, J.P., von Grunau, M.W., & Poulin, C. (1987). Centrifugal organization of direction preferences in the cat's lateral suprasylvian visual cortex and its relation to optic flow field processing. Journal of Neuroscience 7, 943–958.Google Scholar
Saito, H., Yukie, M., Tanaka, K., Hikosaka, K., Fukada, Y., & Iwai, E. (1986). Integration of direction signals of image motion in the superior temporal sulcus of the macaque monkey. Journal of Neuroscience 6(1), 145–157.Google Scholar
Schaafsma, S.J. & Duysens, J. (1996). Neurons in the ventral intraparietal area of awake macaque monkey closely resemble neurons in the dorsal part of the medial superior temporal area in their responses to optic flow patterns. Journal of Neurophysiology 76, 4056–4068.Google Scholar
Schall, J.D. (2002). The neural selection and control of saccades by the frontal eye field. Philosophical Transactions of the Royal Society B (London) 357(1424), 1073–1082.Google Scholar
Schall, J.D., Morel, A., King, D.J., & Bullier, J. (1995). Topography of visual cortex connections with frontal eye field in macaque: Convergence and segregation of processing streams. Journal of Neuroscience 15(6), 4464–4487.Google Scholar
Schmolesky, M.T., Wang, Y., Hanes, D.P., Thompson, K.G., Leutgeb, S., Schall, J.D., & Leventhal, A.G. (1998). Signal timing across the macaque visual system. Journal of Neurophysiology 79(6), 3272–3278.Google Scholar
Segraves, M.A., Goldberg, M.E., Deng, S.Y., Bruce, C.J., Ungerleider, L.G., & Mishkin, M. (1987). The role of striate cortex in the guidance of eye movements in the monkey. Journal of Neuroscience 7, 3040–3058.Google Scholar
Sherk, H. & Fowler, G.A. (2001). Neural analysis of visual information during locomotion. Progress in Brain Research 134, 247–264.Google Scholar
Siegel, R.M.Read, H.L. (1997). Analysis of optic flow in the monkey parietal area 7a. Cerebral Cortex 7(4), 327–346.Google Scholar
Stanton, G.B., Bruce, C.J., & Goldberg, M.E. (1995). Topography of projections to posterior cortical areas from the macaque frontal eye fields. Journal of Comparative Neurology 353(2), 291–305.Google Scholar
Steinmetz, M.A., Motter, B.C., Duffy, C.J., & Mountcastle, V.B. (1987). Functional properties of parietal visual neurons: Radial organization of directionalities within the visual field. Journal of Neuroscience 7(1), 177–191.Google Scholar
Vidyasagar, T.R. & Henry, G.H. (1990). Relationship between preferred orientation and ordinal position in neurons of cat striate cortex. Visual Neuroscience 5, 565–569.Google Scholar
Warren, W.H., Kay, B.A., Duchon, A.P., Zosh, W., & Sahuc, S. (2001). Optic flow is used to control human walking. Nature Neuroscience 4, 213–216.Google Scholar
Wilkie, R.M. & Wann, J.P. (2003). Eye-movements aid the control of locomotion. Journal of Vision 3(11), 677–684.Google Scholar
Wunderlich, G., Marshall, J.C., Amunts, K., Weiss, P.H., Mohlberg, H., Zafiris, O., Zilles, K., & Fink, G.R. (2002). The importance of seeing it coming: A functional magnetic resonance imaging study of motion-in-depth towards the human observer. Neuroscience 112(3), 535–540.Google Scholar
Zar, Z.H. (1999). Biostatistical Analysis, fourth edition. Upper Saddle River, New Jersey: Prentice-Hall Inc.