Hostname: page-component-77c89778f8-gvh9x Total loading time: 0 Render date: 2024-07-17T07:46:23.009Z Has data issue: false hasContentIssue false
  • English
  • Français

Receptive-field structure of optic flow responsive Purkinje cells in the vestibulocerebellum of pigeons

Published online by Cambridge University Press:  09 March 2006

IAN R. WINSHIP  and
DOUGLAS R.W. WYLIE
IAN R. WINSHIP
Affiliation:
Department of Psychology, University of Alberta, Edmonton, Alberta, Canada
DOUGLAS R.W. WYLIE
Affiliation:
Department of Psychology, University of Alberta, Edmonton, Alberta, Canada Centre for Neuroscience, University of Alberta, Edmonton, Alberta, Canada
Get access Rights & Permissions [Opens in a new window]

Abstract

Neurons sensitive to optic flow patterns have been recorded in the the olivo-vestibulocerebellar pathway and extrastriate visual cortical areas in vertebrates, and in the visual neuropile of invertebrates. The complex spike activity (CSA) of Purkinje cells in the vestibulocerebellum (VbC) responds best to patterns of optic flow that result from either self-rotation or self-translation. Previous studies have suggested that these neurons have a receptive-field (RF) structure that “approximates” the preferred optic flowfield with a “bipartite” organization. Contrasting this, studies in invertebrate species indicate that optic flow sensitive neurons are precisely tuned to their preferred flowfield, such that the local motion sensitivities and local preferred directions within their RFs precisely match the local motion in that region of the preferred flowfield. In this study, CSA in the VbC of pigeons was recorded in response to a set of complex computer-generated optic flow stimuli, similar to those used in previous studies of optic flow neurons in primate extrastriate visual cortex, to test whether the receptive field was of a precise or bipartite organization. We found that these RFs were not precisely tuned to optic flow patterns. Rather, we conclude that these neurons have a bipartite RF structure that approximates the preferred optic flowfield by pooling motion subunits of only a few different direction preferences.

Keywords

Optic flowVestibulocerebellumInferior oliveOptokineticReceptive fields
Type
Research Article
Information
Visual Neuroscience , Volume 23 , Issue 1 , January 2006 , pp. 115 - 126
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

Avillac, M., Deneve, S., Olivier, E., Pouget, A., & Duhamel, J.R. (2005). Reference frames for representing visual and tactile locations in parietal cortex. Nature Neuroscience 8, 941–949.Google Scholar
Barnes, W.J.P., Johnson, A.P., Horseman, B.G., & MacAuley, M.W.S. (2002). Computer-aided studies of vision in crabs. Marine and Freshwater Behavioural Physiology35, 1–2, 37–56.
Ben Hamed, S., Duhamel, J.R., Bremmer, F., & Graf, W. (2001). Representation of the visual field in the lateral intraparietal area of macaque monkeys: A quantitative receptive field analysis. Experimental Brain Research 140, 127–144.Google Scholar
Ben Hamed, S., Page, W., Duffy, C., & Pouget, A. (2003). MSTd neuronal basis functions for the population encoding of heading direction. Journal of Neurophysiology 90, 549–558.Google Scholar
Bremmer, F., Duhamel, J.R., Ben Hamed, S., & Graf, W. (2002). Heading encoding in the macaque ventral intraparietal area (VIP). European Journal of Neuroscience 16, 1554–1568.Google Scholar
Burns, S. & Wallman, J. (1981). Relation of single unit properties to the occulomotor function of the nucleus of the basal optic root (AOS) in chickens. Experimental Brain Research 42, 171–180.Google Scholar
Collewijn, H. (1975a). Direction-selective units in the rabbit's nucleus of the optic tract. Brain Research 100, 489–508.Google Scholar
Collewijn, H. (1975b). Oculomotor areas in the rabbit's midbrain and pretectum. Journal of Neurobiology 6, 3–22.Google Scholar
Crowder, N.A., Winship, I.R., & Wylie, D.R. (2000). Topographic organization of inferior olive cells projecting to translational zones in the vestibulocerebellum of pigeons. Journal of Comparative Neurology 419, 87–95.Google Scholar
Dalgaard, P. (2002). Introductory Statistics with R. New York: Springer.
Duffy, C.J. (2004). The cortical analysis of optic flow. In The Visual Neurosciences, Vol. 2, ed. Chalupa, L.M. & Werner, J.S., pp. 1260–1283. Cambridge, Massachusetts: MIT Press.
Duffy, C.J. & Wurtz, R.H. (1991a). Sensitivity of MST neurons to optic flow stimuli. I. A continuum of response selectivity to large-field stimuli. Journal of Neurophysiology 65, 1329–1345.Google Scholar
Duffy, C.J. & Wurtz, R.H. (1991b). Sensitivity of MST neurons to optic flow stimuli. II. Mechanisms of response selectivity revealed by small-field stimuli. Journal of Neurophysiology 65, 1346–1359.Google Scholar
Duffy, C.J. & Wurtz, R.H. (1995). Response of monkey MST neurons to optic flow stimuli with shifted centers of motion. Journal of Neuroscience 15, 5192–5208.Google Scholar
Duhamel, J.R., Bremmer, F., Ben Hamed, S., & Graf, W. (1997). Spatial invariance of visual receptive fields in parietal cortex neurons. Nature 389, 845–848.Google Scholar
Efron, B. & Tibshirani, R.J. (1994). Introduction to the Bootstrap. New York: Chapman & Hall.
Erichsen, J.T., Hodos, W., Evinger, C., Bessette, B.B., & Philips, S.J. (1989). Head orientation in pigeons: Postural, locomotor, and visual determinants. Brain, Behaviour, and Evolution 33, 268–578.Google Scholar
Fite, K.V. (1985). Pretectal and accessory-optic visual nuclei of fish, amphibia and reptiles: Themes and variations. Brain, Behaviour, and Evolution 26, 71–90.Google Scholar
Gibson, J.J. (1954). The visual perception of objective motion and subjective movement. Psychological Review 61, 304–314.Google Scholar
Graf, W., Simpson, J.I., & Leonard, C.S. (1988). Spatial organization of visual messages of the rabbit's cerebellar flocculus. II. Complex and simple spike responses of Purkinje cells. Journal of Neurophysiology 60, 2091–2021.Google Scholar
Grasse, K.L. & Cynader, M.S. (1982). Electrophysiology of medial terminal nucleus of accessory optic system in the cat. Journal of Neurophysiology 48, 490–504.Google Scholar
Grasse, K.L., Cyander, M.S., & Douglas, R.M. (1984). Alterations in response properties in the lateral and dorsal terminal nuclei of the cat accessory optic system following visual cortex lesions. Experimental Brain Research 55, 69–80.Google Scholar
Graziano, M.S., Andersen, R.A., & Snowden, R.J. (1994). Tuning of MST neurons to spiral motions. Journal of Neuroscience 14, 54–67.Google Scholar
Hengstenberg, R. (1993). Multisensory control in insect oculomotor systems. In Visual Motion and Its Role in the Stabilization of Gaze, ed. Miles, F.A., pp. 285–298. New York: Elsevier.
Ibbotson, M.R., Mark, R.F., & Maddess, T.L. (1994). Spatiotemporal response properties of direction-selective neurons in the nucleus of the optic tract and the dorsal terminal nucleus of the wallaby, Macropus eugenii. Journal of Neurophysiology 72, 2927–2943.Google Scholar
Johnson, A.P., Horseman, B.G., MacAuley, M.W.S., & Barnes, W.J.P. (2002). PC-based visual stimuli for behavioural and electrophysiological studies of optic flow field detection. Journal of Neuroscience Methods114, 1, 51–61.
Kano, M., Kano, M.-S., Kusunoki, M., & Maekawa, K. (1990a). Nature of the optokinetic response and zonal organization of climbing fibre afferents in the vestibulocerebellum of the pigmented rabbit. Experimental Brain Research 80, 238–251.Google Scholar
Kano, M., Kano, M.-S., & Maekawa, K. (1990b). Receptive field organization of climbing fibre afferents responding to optokinetic stimulation in the cerebellar nodulus and flocculus of the pigmented rabbit. Experimental Brain Research 82, 499–512.Google Scholar
Karmeier, K., Krapp, H.G., & Egelhaaf, M. (2003). Robustness of the tuning of fly visual interneurons to rotatory optic flow. Journal of Neurophysiology 90, 1626–1634.Google Scholar
Karten, H.J. & Hodos, W. (1967). A Stereotaxic Atlas of the Brain of the Pigeon (Columba Livia). Baltimore, Maryland: Johns Hopkins Press.
Koenderink, J.J. & van Doorn, A.J. (1987). Facts on optic flow. Biological Cybernetics 56, 247–254.Google Scholar
Kogo, N., McGartland Rubio, D., & Arial, M. (1998). Direction tuning of individual retinal inputs to the turtle accessory optic system. Journal of Neuroscience 18, 2673–2684.Google Scholar
Krapp, H.G. & Hengstenberg, B. (1996). Estimation of self-motion by optic flow processing in single visual interneurons. Nature 384, 463–466.Google Scholar
Krapp, H.G., Hengstenberg, B., & Hengstenberg, R. (1998). Dendritic structure and receptive-field organization of optic flow processing interneurons in the fly. Journal of Neurophysiology 79, 1902–1917.Google Scholar
Kusunoki, M., Kan, M., Kano, M.-S., & Maekawa, K. (1990). Nature of optokinetic response and zonal organization of climbing fibre afferents in the vestibulocerebellum of the pigmented rabbit. I. The flocculus. Experimental Brain Research 80, 225–237.Google Scholar
Lagae, L., Maes, H., Raiguel, S., Xiao, D.K., & Orban, G.A. (1994). Responses of macaque STS neurons to optic flow components: A comparison of areas MT and MST. Journal of Neurophysiology 71, 1597–1626.Google Scholar
Lappe, M., Bremmer, F., Pekel, M., Thiele, A., & Hoffman, K.P. (1996). Optic flow processing in monkey STS: A theoretical and experimental approach. Journal of Neuroscience 16, 6265–6285.Google Scholar
Leonard, C.S., Simpson, J.I., & Graf, W. (1988). Spatial organization of visual messages of the rabbit's cerebellar flocculus. I. Typology of inferior olive neurons of the dorsal cap of Kooy. Journal of Neurophysiology 60, 2073–2090.Google Scholar
McKenna, O.C. & Wallman, J. (1985). Accessory optic system and pretectum of birds: Comparisons with those of other vertebrates. Brain, Behaviour, and Evolution 26, 91–116.Google Scholar
Motter, B.C., Steinmetz, M.A., Duffy, C.J., & Mountcastle, V.B. (1987). Functional properties of parietal visual neurons: Mechanisms of directionality along a single axis. Journal of Neuroscience 7, 154–176.Google Scholar
Mustari, M.J. & Fuchs, A.F. (1990). Discharge patterns of neurons in the pretectal nucleus of the optic tract (NOT) in the behaving primate. Journal of Neurophysiology 64, 77–90.Google Scholar
Nakayama, K. & Loomis, J.M. (1974). Optical velocity patterns, velocity-sensitive neurons, and space perception: A hypothesis. Perception 3, 63–80.Google Scholar
Orban, G.A., Lagae, L., Verri, A., Raiguel, S., Xiao, D., Maes, H., & Torre, V. (1992). First-order analysis of optical flow in monkey brain. Proceedings of the National Academy of Sciences of the U.S.A. 89, 2595–2599.Google Scholar
Oyster, C.W., Simpson, J.I., Takahashi, E.S., & Soodak, R.E. (1980). Retinal ganglion cells projecting to the rabbit accessory optic system. Journal of Comparative Neurology 190, 49–61.Google Scholar
Page, W. & Duffy, C. (2003). Heading representation in MST: Sensory interactions and population encoding. Journal of Neurophysiology 89, 1994–2013.Google Scholar
R Development Core Team. (2005). R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. http://www.R-project.org.
Rosenberg, A.F. & Ariel, M. (1990). Visual-response properties of neurons in turtle basal optic nucleus in vitro. Journal of Neurophysiology 63, 1033–1045.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, 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
Simpson, J.I. (1984). The accessory optic system. Annual Review of Neuroscience 7, 13–41.Google Scholar
Simpson, J.I. & Alley, K.E. (1974). Visual climbing fiber input to rabbit vestibulo-cerebellum: A source of direction-specific information. Brain Research 82, 302–308.Google Scholar
Simpson, J.I., Giolli, R.A., & Blanks, R.H. (1988c). The pretectal nuclear complex and the accessory optic system. Reviews of Oculomotor Research 2, 335–364.Google Scholar
Simpson, J.I., Graf, W., & Leonard, C. (1981). The coordinate system of visual climbing fibres to the flocculus. In Progress in Oculomotor Research, ed. Fuchs, A.F. & Becker, W., pp. 475–484. Amsterdam: Elsevier.
Simpson, J.I., Graf, W., & Leonard, C. (1989). Three-dimensional representation of retinal image movement by climbing fiber activity. In The Olivocerebellar System in Motor Control: Experimental Brain Research Supplement, Vol. 17, ed. Strata, P., pp. 323–327. Heidelberg: Springer-Verlag.
Simpson, J.I., Leonard, C.S., & Soodak, R.E. (1988a). The accessory optic system of rabbit. II. Spatial organization of direction selectivity. Journal of Neurophysiology 60, 2055–2072.Google Scholar
Simpson, J.I., Leonard, C.S., & Soodak, R.E. (1988b). The accessory optic system: Analyzer of self-motion. Annals of the New York Academy of Sciences 545, 170–179.Google Scholar
Simpson, J.I., Soodak, R.E., & Hess, R. (1979). The accessory optic system and its relation to the vestibulocerebellum. Progress in Brain Research 50, 715–724.Google Scholar
Soodak, R.E. & Simpson, J.I. (1988). The accessory optic system of rabbit. I. Basic visual response properties. Journal of Neurophysiology 60, 2055–2072.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, 177–191.Google Scholar
Tanaka, K., Fukada, Y., & Saito, H.A. (1989). 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. Journal of Neurophysiology 62, 642–656.Google Scholar
Tanaka, K., Hikosaka, K., Saito, H., Yukie, M., Fukada, Y., & Iwai, E. (1986). Analysis of local and wide-field movements in the superior temporal visual areas of the macaque monkey. Journal of Neuroscience 6, 134–144.Google Scholar
Tanaka, K. & Saito, H. (1989). 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. Journal of Neurophysiology 62, 626–641.Google Scholar
Vogels, R. & Orban, G.A. (1994). Activity of inferior temporal neurons during orientation discrimination with successively presented gratings. Journal of Neurophysiology 71, 1428–1451.Google Scholar
Weber, J.T. (1985). Pretectal complex and accessory optic system in alert monkeys. Brain, Behaviour, and Evolution 26, 117–140.Google Scholar
Winship, I.R., Hurd, P.L., & Wylie, D.R.W. (2005). Spatio-temporal tuning of optic flow inputs to the vestibulocerebellum in pigeons: Differences between mossy and climbing fibre pathways. Journal of Neurophysiology 93, 1266–1277.Google Scholar
Winship, I.R. & Wylie, D.R.W. (2001). Responses of neurons in the medial column of the inferior olive in pigeons to translational and rotational optic flowfields. Experimental Brain Research 141, 63–78.Google Scholar
Winship, I.R. & Wylie, D.R.W. (2003). Zonal organization of the vestibulocerebellum in pigeons (Columba livia): I. Climbing fibre input to the flocculus. Journal of Comparative Neurology 456, 127–139.Google Scholar
Winterson, B.J. & Brauth, S.E. (1985). Direction-selective single units in the nucleus lentiformis mesencephali of the pigeon (Columba livia). Experimental Brain Research 60, 215–226.Google Scholar
Wylie, D.R.W. (2001). Projections from the nucleus of the basal optic root and nucleus lentiformis mesencephali to the inferior olive in pigeons (Columba livia). Journal of Comparative Neurology 429, 502–513.Google Scholar
Wylie, D.R.W., Bischof, W.F., & Frost, B.J. (1998). Common reference frame for neural coding of translational and rotational optic flow. Nature 392, 278–282.Google Scholar
Wylie, D.R.W., Brown, M.R., Barkley, R.R., Winship, I.R., Crowder, N.A., & Todd, K.G. (2003a). Zonal organization the vestibulocerebellum in pigeons (Columba livia): II. Projections of the rotation zones of the flocculus. Journal of Comparative Neurology 456, 140–153.Google Scholar
Wylie, D.R.W., Brown, M.R., Winship, I.R., Crowder, N.A., & Todd, K.G. (2003b). Zonal organization of the vestibulocerebellum in pigeons (Columba livia): III. Projections of the translation zones of the ventral uvula and nodulus. Journal of Comparative Neurology 465, 179–194.Google Scholar
Wylie, D.R. & Crowder, N.A. (2000). Spatiotemporal properties of fast and slow neurons in the pretectal nucleus lentiformis mesencephali in pigeons. Journal of Neurophysiology 84, 2529–2540.Google Scholar
Wylie, D.R. & Frost, B.J. (1990). Binocular neurons in the nucleus of the basal optic root (nBOR) of the pigeon are selective for either translational or rotational visual flow. Visual Neuroscience 5, 489–495.Google Scholar
Wylie, D.R. & Frost, B.J. (1993). Responses of pigeon vestibulocerebellar neurons to optokinetic stimulation: II. The 3-dimensional reference frame of rotation neurons in the flocculus. Journal of Neurophysiology 70, 2647–2659.Google Scholar
Wylie, D.R.W. & Frost, B.J. (1996). The pigeon optokinetic system: Visual input in extraocular muscle coordinates. Visual Neuroscience 13, 945–953.Google Scholar
Wylie, D.R.W. & Frost, B.J. (1999a). Complex spike activity of Purkinje cells in the ventral uvula and nodulus of pigeons in response to translational optic flowfields. Journal of Neurophysiology 81, 256–266.Google Scholar
Wylie, D.R. & Frost, B.J. (1999b). Responses of neurons in the nucleus of the basal optic root to translational and rotational flowfields. Journal of Neurophysiology 81, 267–276.Google Scholar
Wylie, D.R., Kripalani, T.-K., & Frost, B.J. (1993). Responses of pigeon vestibulocerebellar neurons to optokinetic stimulation: I. Functional organization of neurons discriminating between translational and rotational visual flow. Journal of Neurophysiology 70, 2632–2646.Google Scholar