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Organization of the cerebellum: Correlating zebrin immunochemistry with optic flow zones in the pigeon flocculus

  • JANELLE M.P. PAKAN (a1), DAVID J. GRAHAM (a1), CRISTIÁN GUTIÉRREZ-IBÁÑEZ (a1) and DOUGLAS R. WYLIE (a1) (a2)

Abstract

The cerebellar cortex has a fundamental parasagittal organization that is apparent in the physiological response properties of Purkinje cells (PCs) and the expression of several molecular markers such as zebrin II (ZII). ZII is heterogeneously expressed in PCs such that there are sagittal stripes of high expression [ZII immunopositive (ZII+)] interdigitated with stripes of little or no expression [ZII immunonegative (ZII−)]. Several studies in rodents have suggested that climbing fiber (CF) afferents from an individual subnucleus in the inferior olive project to either ZII+ or ZII− stripes but not both. In this report, we show that this is not the case in the pigeon flocculus. The flocculus (the lateral half of folia IXcd and X) receives visual-optokinetic information and is important for generating compensatory eye movements to facilitate gaze stabilization. Previous electrophysiological studies from our lab have shown that the pigeon flocculus consists of four parasagittal zones: 0, 1, 2, and 3. PC complex spike activity (CSA), which reflects CF input, in zones 0 and 2 responds best to rotational optokinetic stimuli about the vertical axis (VA zones), whereas CSA in zones 1 and 3 responds best to rotational optokinetic stimuli about the horizontal axis (HA zones). In addition, folium IXcd consists of seven pairs of ZII+/− stripes. Here, we recorded CSA of floccular PCs to optokinetic stimuli, marked recording locations, and subsequently visualized ZII expression in the flocculus. VA neurons were localized to the P4+/− and P6+/− stripes and HA neurons were localized to the P5+/− and P7− stripes. This is the first study showing that a series of adjacent ZII+/− stripes are tied to specific physiological functions as measured in the responses of PCs to natural stimulation. Moreover, this study shows that the functional zone in the pigeon flocculus spans a ZII+/− stripe pair, which is contrary to the scheme proposed from rodent research.

Copyright

Corresponding author

*Address correspondence and reprint requests to: Douglas R. Wylie, Department of Psychology, University of Alberta, Edmonton, Alberta, Canada T6G 2E9. E-mail: dwylie@ualberta.ca

References

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Ahn, A.H., Dziennis, S., Hawkes, R. & Herrup, K. (1994). The cloning of zebrin II reveals its identity with aldolase C. Development 120, 20812090.
Akintunde, A. & Eisenman, L.M. (1994). External cuneocerebellar projection and Purkinje cell zebrin II bands: A direct comparison of parasagittal banding in the mouse cerebellum. Journal of Chemical Neuroanatomy 7, 7586.
Andersson, G. & Oscarsson, O. (1978). Climbing fiber microzones in cerebellar vermis and their projection to different groups of cells in the lateral vestibular nucleus. Experimental Brain Research 32, 565579.
Apps, R. & Garwicz, M. (2005). Anatomical and physiological foundations of cerebellar information processing. Nature Reviews. Neuroscience 6, 297311.
Apps, R. & Hawkes, R. (2009). Cerebellar cortical organization: A one-map hypothesis. Nature Reviews. Neuroscience 10, 670681.
Armstrong, C.L., Krueger-Naug, A.M., Currie, R.W. & Hawkes, R. (2000). Constitutive expression of the 25-kDa heat shock protein Hsp25 reveals novel parasagittal bands of purkinje cells in the adult mouse cerebellar cortex. The Journal of Comparative Neurology 416, 383397.
Barmack, N.H., & Yakhnitsa, V. (2003). Cerebellar climbing fibers modulate simple spikes in Purkinje cells. The Journal of Neuroscience 23, 79047916.
Barmack, N.H., & Yakhnitsa, V. (2008). Distribution of granule cells projecting to focal Purkinje cells in mouse uvula-nodulus. Neuroscience 156, 216221.
Brecha, N., Karten, H.J. & Hunt, S.P. (1980). Projections of the nucleus of the basal optic root in the pigeon: An autoradiographic and horseradish peroxidase study. The Journal of Comparative Neurology 189, 615670.
Brochu, G., Maler, L. & Hawkes, R. (1990). Zebrin II: A polypeptide antigen expressed selectively by Purkinje cells reveals compartments in rat and fish cerebellum. The Journal of Comparative Neurology 291, 538552.
Chockkan, V. & Hawkes, R. (1994). Functional and antigenic maps in the rat cerebellum: Zebrin compartmentation and vibrissal receptive fields in lobule IXa. The Journal of Comparative Neurology 345, 3345.
Clarke, P.G. (1977). Some visual and other connections to the cerebellum of the pigeon. The Journal of Comparative Neurology 174, 535552.
De Zeeuw, C.I., Wylie, D.R., DiGiorgi, P.L. & Simpson, J.I. (1994). Projections of individual Purkinje cells of identified zones in the flocculus to the vestibular and cerebellar nuclei in the rabbit. The Journal of Comparative Neurology 349, 428447.
Eccles, J.C., Llinas, R. & Sasaki, K. (1966). Intracellularly recorded responses of the cerebellar Purkinje cells. Experimental Brain Research 1, 161183.
Eisenman, L.M. & Hawkes, R. (1993). Antigenic compartmentation in the mouse cerebellar cortex: Zebrin and HNK-1 reveal a complex, overlapping molecular topography. The Journal of Comparative Neurology 335, 586605.
Ekerot, C.F. & Larson, B. (1973). Correlation between sagittal projection zones of climbing and mossy fibre paths in cat cerebellar anterior lobe. Brain Research 64, 446450.
Freedman, S.L., Feirabend, H.K., Vielvoye, G.J. & Voogd, J. (1975). Re-examination of the ponto-cerebellar projection in the adult white leghorn (Gallus domesticus). Acta Morphologica Neerlando-Scandinavica, 13, 236238.
Fujita, H., Oh-Nishi, A., Obayashi, S. & Sugihara, I. (2010). Organization of the marmoset cerebellum in three-dimensional space: Lobulation, aldolase C compartmentalization and axonal projection. The Journal of Comparative Neurology 518, 17641791.
Gao, W., Chen, G., Reinert, K.C. & Ebner, T.J. (2006). Cerebellar cortical molecular layer inhibition is organized in parasagittal zones. The Journal of Neuroscience 26, 83778387.
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, 20912121.
Gravel, C., Eisenman, L.M., Sasseville, R. & Hawkes, R. (1987). Parasagittal organization of the rat cerebellar cortex: Direct correlation between antigenic Purkinje cell bands revealed by mabQ113 and the organization of the olivocerebellar projection. The Journal of Comparative Neurology 265, 294310.
Gravel, C. & Hawkes, R. (1990). Parasagittal organization of the rat cerebellar cortex: Direct comparison of Purkinje cell compartments and the organization of the spinocerebellar projection. The Journal of Comparative Neurology 291, 79102.
Hawkes, R. & Gravel, C. (1991). The modular cerebellum. Progress in Neurobiology 36, 309327.
Hawkes, R. & Herrup, K. (1995). Aldolase C/zebrin II and the regionalization of the cerebellum. Journal of Molecular Neuroscience 6, 147158.
Herrup, K. & Kuemerle, B. (1997). The compartmentalization of the cerebellum. Annual Review of Neuroscience 20, 6190.
Iwaniuk, A.N., Marzban, H., Pakan, J.M., Watanabe, M., Hawkes, R. & Wylie, D.R. (2009). Compartmentation of the cerebellar cortex of hummingbirds (Aves: Trochilidae) revealed by the expression of zebrin II and phospholipase C beta 4. Journal of Chemical Neuroanatomy 37, 5563.
Ji, Z. & Hawkes, R. (1994). Topography of Purkinje cell compartments and mossy fiber terminal fields in lobules II and III of the rat cerebellar cortex: Spinocerebellar and cuneocerebellar projections. Neuroscience 61, 935954.
Kano, M.S., Kano, M. & Maekawa, K. (1990). Receptive field organization of climbing fiber afferents responding to optokinetic stimulation in the cerebellar nodulus and flocculus of the pigmented rabbit. Experimental Brain Research 82, 499512.
Karten, H. & Hodos, W. (1967). A Stereotaxic Atlas of the Brain of the Pigeon (Columba livia). Baltimore, MD: Johns Hopkins Press.
Larouche, M. & Hawkes, R. (2006). From clusters to stripes: The developmental origins of adult cerebellar compartmentation. Cerebellum 5, 7788.
Llinas, R. & Sasaki, K. (1989). The functional organization of the olivo-cerebellar system as examined by multiple Purkinje cell recordings. The European Journal of Neuroscience 1, 587602.
Marzban, H., Chung, S.H., Pezhouh, M.K., Feirabend, H., Watanabe, M., Voogd, J. & Hawkes, R. (2010). Antigenic compartmentation of the cerebellar cortex in the chicken (Gallus domesticus). The Journal of Comparative Neurology 518, 22212239.
Matsushita, M., Ragnarson, B. & Grant, G. (1991). Topographic relationship between sagittal Purkinje cell bands revealed by a monoclonal antibody to zebrin I and spinocerebellar projections arising from the central cervical nucleus in the rat. Experimental Brain Research 84, 133141.
Miles, F.A. & Lisberger, S.G. (1981). Plasticity in the vestibulo-ocular reflex: A new hypothesis. Annual Review of Neuroscience 4, 273299.
Mostofi, A., Holtzman, T. Grout, A.S., Yeo, C.H. & Edgley, S.A. (2010). Electrophysiological localization of eyeblink-related microzones in rabbit cerebellar cortex. The Journal of Neuroscience 30, 89208930.
Nagao, S., Kitazawa, H., Osanai, R. & Hiramatsu, T. (1997). Acute effects of tetrahydrobiopterin on the dynamic characteristics and adaptability of of vestibulo-ocular reflex in normal and flocculus lesioned rabbits. Neuroscience Letters 231, 4144.
Necker, R. (1992). Spinal neurons projecting to anterior or posterior cerebellum in the pigeon. Anatomy & Embryology (Berlin) 185, 325334.
Ozol, K., Hayden, J.M., Oberdick, J. & Hawkes, R. (1999). Transverse zones in the vermis of the mouse cerebellum. The Journal of Comparative Neurology 412, 95111.
Pakan, J.M., Graham, D.J. & Wylie, D.R. (2010). Organization of visual mossy fiber projections and zebrin expression in the pigeon vestibulocerebellum. The Journal of Comparative Neurology 518, 175198.
Pakan, J.M., Iwaniuk, A.N., Wylie, D.R., Hawkes, R. & Marzban, H. (2007). Purkinje cell compartmentation as revealed by zebrin II expression in the cerebellar cortex of pigeons (Columba livia). The Journal of Comparative Neurology 501, 619630.
Pakan, J.M., Todd, K.G., Nguyen, A.P., Winship, I.R., Hurd, P.L., Jantzie, L.L. & Wylie, D.R. (2005). Inferior olivary neurons innervate multiple zones of the flocculus in pigeons (Columba livia). The Journal of Comparative Neurology 486, 159168.
Pakan, J.M. & Wylie, D.R. (2008). Congruence of zebrin II expression and functional zones defined by climbing fiber topography in the flocculus. Neuroscience 157, 5769.
Paukert, M., Huang, Y.H., Tanaka, K., Rothstein, J.D. & Bergles, D.E. (2010). Zones of enhanced glutamate release from climbing fibers in the mammalian cerebellum. The Journal of Neuroscience 30, 72907299.
Pijpers, A., Apps, R., Pardoe, J., Voogd, J. & Ruigrok, T.J. (2006). Precise spatial relationships between mossy fibers and climbing fibers in rat cerebellar cortical zones. The Journal of Neuroscience 26, 1206712080.
Ruigrok, T.J. (2003). Collateralization of climbing and mossy fibers projecting to the nodulus and flocculus of the rat cerebellum. The Journal of Comparative Neurology 466, 278298.
Ruigrok, T.J., Pijpers, A., Goedknegt-Sabel, E. & Coulon, P. (2008). Multiple cerebellar zones are involved in the control of individual muscles: A retrograde transneuronal tracing study with rabies virus in the rat. European Journal of Neuroscience 28, 181200.
Schonewille, M., Luo, C., Ruigrok, T.J., Voogd, J., Schmolesky, M.T., Rutteman, M., Hoebeek, F.E., De Jeu, M.T. & De Zeeuw, C.I. (2006). Zonal organization of the mouse flocculus: Physiology, input, and output. The Journal of Comparative Neurology 497, 670682.
Schwarz, I.E. & Schwarz, D.W. (1983). The primary vestibular projection to the cerebellar cortex in the pigeon (Columba livia). The Journal of Comparative Neurology 216, 438444.
Sillitoe, R.V. & Hawkes, R. (2002). Whole-mount immunohistochemistry: A high-throughput screen for patterning defects in the mouse cerebellum. The Journal of Histochemistry & Cytochemistry 50, 235244.
Sillitoe, R.V., Marzban, H., Larouche, M., Zahedi, S., Affanni, J. & Hawkes, R. (2005). Conservation of the architecture of the anterior lobe vermis of the cerebellum across mammalian species. Progress in Brain Research 148, 283297.
Simpson, J., Graf, W. & Leonard, C.L. (1981). The coordinate system of visual climbing fibres to the flocculus. In Progress in Oculomotor Research, Amsterdam, The Netherlands: Elsevier.
Sugihara, I., Fujita, H., Na, J., Quy, P.N., Li, B.Y. & Ikeda, D. (2009). Projection of reconstructed single Purkinje cell axons in relation to the cortical and nuclear aldolase C compartments of the rat cerebellum. The Journal of Comparative Neurology 512, 282304.
Sugihara, I., Marshall, S.P. & Lang, E.J. (2007). Relationship of complex spike synchrony bands and climbing fiber projection determined by reference to aldolase C compartments in crus IIa of the rat cerebellar cortex. The Journal of Comparative Neurology 501, 1329.
Sugihara, I. & Quy, P.N. (2007). Identification of aldolase C compartments in the mouse cerebellar cortex by olivocerebellar labeling. The Journal of Comparative Neurology 500, 10761092.
Sugihara, I. & Shinoda, Y. (2004). Molecular, topographic, and functional organization of the cerebellar cortex: A study with combined aldolase C and olivocerebellar labeling. The Journal of Neuroscience 24, 87718785.
Sugihara, I. & Shinoda, Y. (2007). Molecular, topographic, and functional organization of the cerebellar nuclei: Analysis by three-dimensional mapping of the olivonuclear projection and aldolase C labeling. The Journal of Neuroscience 27, 96969710.
Vielvoye, G.J. & Voogd, J. (1977). Time dependence of terminal degeneration in spino-cerebellar mossy fiber rosettes in the chicken and the application of terminal degeneration in successive degeneration experiments. The Journal of Comparative Neurology 175, 233242.
Voogd, J. (1967). Comparative aspects of the structure and fibre connexions of the mammalian cerebellum. Progress in Brain Research 25, 94134.
Voogd, J. & Bigaré, F. (1980). Topographical distribution of olivary and cortico nuclear fibers in the cerebellum: A review. In The Inferior Olivary Nucleus: Anatomy and Physiology, ed. Courville, J., de Montigny, C. & Lamarre, Y., pp. 207234. New York: Raven Press.
Voogd, J., Broere, G. & van Rossum, J. (1969). The medio-lateral distribution of the spinocerebellar projection in the anterior lobe and the simple lobule in the cat and a comparison with some other afferent fibre systems. Psychiatria, Neurologia, Neurochirurgia 72, 137151.
Voogd, J. & Glickstein, M. (1998). The anatomy of the cerebellum. Trends in Neurosciences 21, 370375.
Voogd, J., Pardoe, J., Ruigrok, T.J. & Apps, R. (2003). The distribution of climbing and mossy fiber collateral branches from the copula pyramidis and the paramedian lobule: Congruence of climbing fiber cortical zones and the pattern of zebrin banding within the rat cerebellum. The Journal of Neuroscience 23, 46454656.
Voogd, J. & Ruigrok, T.J. (2004). The organization of the corticonuclear and olivocerebellar climbing fiber projections to the rat cerebellar vermis: The congruence of projection zones and the zebrin pattern. Journal of Neurocytology 33, 521.
Voogd, J. & Wylie, D.R. (2004). Functional and anatomical organization of floccular zones: A preserved feature in vertebrates. The Journal of Comparative Neurology 470, 107112.
Wadiche, J.I. & Jahr, C.E. (2005). Patterned expression of Purkinje cell glutamate transporters controls synaptic plasticity. Nature Neuroscience 8, 13291334.
Waespe, W. & Henn, V. (1987). Gaze stabilization in the primate. The interaction of the vestibulo-ocular reflex, optokinetic nystagmus, and smooth pursuit. Reviews of Physiology, Biochemistry & Pharmacology 106, 37125.
Winship, I.R. & Wylie, D.R. (2001). Responses of neurons in the medial column of the inferior olive in pigeons to translational and rotational optic flowfields. Experimental Brain Research 141, 6378.
Winship, I.R. & Wylie, D.R. (2003). Zonal organization of the vestibulocerebellum in pigeons (Columba livia): I. Climbing fiber input to the flocculus. The Journal of Comparative Neurology 456, 127139.
Wu, H.S., Sugihara, I. & Shinoda, Y. (1999). Projection patterns of single mossy fibers originating from the lateral reticular nucleus in the rat cerebellar cortex and nuclei. The Journal of Comparative Neurology 411, 97118.
Wylie, D.R. (2001). Projections from the nucleus of the basal optic root and nucleus lentiformis mesencephali to the inferior olive in pigeons (Columba livia). The Journal of Comparative Neurology 429, 502513.
Wylie, D.R., Brown, M.R., Barkley, R.R., Winship, I.R., Crowder, N.A. & Todd, K.G. (2003). Zonal organization of the vestibulocerebellum in pigeons (Columba livia): II. Projections of the rotation zones of the flocculus. The Journal of Comparative Neurology 456, 140153.
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, 26472659.
Wylie, D.R., Kripalani, T. & 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, 26322646.
Wylie, D.R., Winship, I.R. & Glover, R.G. (1999). Projections from the medial column of the inferior olive to different classes of rotation-sensitive Purkinje cells in the flocculus of pigeons. Neuroscience Letters 268, 97100.

Keywords

Organization of the cerebellum: Correlating zebrin immunochemistry with optic flow zones in the pigeon flocculus

  • JANELLE M.P. PAKAN (a1), DAVID J. GRAHAM (a1), CRISTIÁN GUTIÉRREZ-IBÁÑEZ (a1) and DOUGLAS R. WYLIE (a1) (a2)

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