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

Published online by Cambridge University Press:  04 April 2011

JANELLE M.P. PAKAN ,
DAVID J. GRAHAM ,
CRISTIÁN GUTIÉRREZ-IBÁÑEZ  and
DOUGLAS R. WYLIE
JANELLE M.P. PAKAN
Affiliation:
Department of Neuroscience, Centre for Neuroscience, University of Alberta, Edmonton, Alberta, Canada
DAVID J. GRAHAM
Affiliation:
Department of Neuroscience, Centre for Neuroscience, University of Alberta, Edmonton, Alberta, Canada
CRISTIÁN GUTIÉRREZ-IBÁÑEZ
Affiliation:
Department of Neuroscience, Centre for Neuroscience, University of Alberta, Edmonton, Alberta, Canada
DOUGLAS R. WYLIE*
Affiliation:
Department of Neuroscience, Centre for Neuroscience, University of Alberta, Edmonton, Alberta, Canada Department of Psychology, University of Alberta, Edmonton, Alberta, Canada
*
*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
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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.

Keywords

OptokineticVestibulocerebellumClimbing fiberCompartmentationAldolase C
Type
Research Articles
Information
Visual Neuroscience , Volume 28 , Issue 2 , March 2011 , pp. 163 - 174
Copyright
Copyright © Cambridge University Press 2011

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References

Ahn, A.H., Dziennis, S., Hawkes, R. & Herrup, K. (1994). The cloning of zebrin II reveals its identity with aldolase C. Development 120, 2081–2090.CrossRefGoogle ScholarPubMed
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, 75–86.CrossRefGoogle ScholarPubMed
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, 565–579.Google ScholarPubMed
Apps, R. & Garwicz, M. (2005). Anatomical and physiological foundations of cerebellar information processing. Nature Reviews. Neuroscience 6, 297–311.CrossRefGoogle ScholarPubMed
Apps, R. & Hawkes, R. (2009). Cerebellar cortical organization: A one-map hypothesis. Nature Reviews. Neuroscience 10, 670–681.CrossRefGoogle ScholarPubMed
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, 383–397.3.0.CO;2-M>CrossRefGoogle ScholarPubMed
Barmack, N.H., & Yakhnitsa, V. (2003). Cerebellar climbing fibers modulate simple spikes in Purkinje cells. The Journal of Neuroscience 23, 7904–7916.CrossRefGoogle ScholarPubMed
Barmack, N.H., & Yakhnitsa, V. (2008). Distribution of granule cells projecting to focal Purkinje cells in mouse uvula-nodulus. Neuroscience 156, 216–221.CrossRefGoogle ScholarPubMed
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, 615–670.CrossRefGoogle ScholarPubMed
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, 538–552.CrossRefGoogle ScholarPubMed
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, 33–45.CrossRefGoogle ScholarPubMed
Clarke, P.G. (1977). Some visual and other connections to the cerebellum of the pigeon. The Journal of Comparative Neurology 174, 535–552.CrossRefGoogle Scholar
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, 428–447.CrossRefGoogle Scholar
Eccles, J.C., Llinas, R. & Sasaki, K. (1966). Intracellularly recorded responses of the cerebellar Purkinje cells. Experimental Brain Research 1, 161–183.CrossRefGoogle ScholarPubMed
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, 586–605.CrossRefGoogle ScholarPubMed
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, 446–450.CrossRefGoogle ScholarPubMed
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, 236–238.Google ScholarPubMed
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, 1764–1791.CrossRefGoogle ScholarPubMed
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, 8377–8387.CrossRefGoogle ScholarPubMed
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, 2091–2121.CrossRefGoogle ScholarPubMed
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, 294–310.CrossRefGoogle ScholarPubMed
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, 79–102.CrossRefGoogle ScholarPubMed
Hawkes, R. & Gravel, C. (1991). The modular cerebellum. Progress in Neurobiology 36, 309–327.CrossRefGoogle ScholarPubMed
Hawkes, R. & Herrup, K. (1995). Aldolase C/zebrin II and the regionalization of the cerebellum. Journal of Molecular Neuroscience 6, 147–158.CrossRefGoogle ScholarPubMed
Herrup, K. & Kuemerle, B. (1997). The compartmentalization of the cerebellum. Annual Review of Neuroscience 20, 61–90.CrossRefGoogle ScholarPubMed
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, 55–63.CrossRefGoogle ScholarPubMed
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, 935–954.CrossRefGoogle ScholarPubMed
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, 499–512.CrossRefGoogle ScholarPubMed
Karten, H. & Hodos, W. (1967). A Stereotaxic Atlas of the Brain of the Pigeon (Columba livia). Baltimore, MD: Johns Hopkins Press.Google Scholar
Larouche, M. & Hawkes, R. (2006). From clusters to stripes: The developmental origins of adult cerebellar compartmentation. Cerebellum 5, 77–88.CrossRefGoogle ScholarPubMed
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, 587–602.CrossRefGoogle ScholarPubMed
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, 2221–2239.CrossRefGoogle ScholarPubMed
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, 133–141.CrossRefGoogle ScholarPubMed
Miles, F.A. & Lisberger, S.G. (1981). Plasticity in the vestibulo-ocular reflex: A new hypothesis. Annual Review of Neuroscience 4, 273–299.CrossRefGoogle ScholarPubMed
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, 8920–8930.CrossRefGoogle ScholarPubMed
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, 41–44.CrossRefGoogle ScholarPubMed
Necker, R. (1992). Spinal neurons projecting to anterior or posterior cerebellum in the pigeon. Anatomy & Embryology (Berlin) 185, 325–334.CrossRefGoogle ScholarPubMed
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, 95–111.3.0.CO;2-Y>CrossRefGoogle ScholarPubMed
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, 175–198.CrossRefGoogle ScholarPubMed
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, 619–630.CrossRefGoogle ScholarPubMed
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, 159–168.CrossRefGoogle ScholarPubMed
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, 57–69.CrossRefGoogle ScholarPubMed
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, 7290–7299.CrossRefGoogle ScholarPubMed
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, 12067–12080.CrossRefGoogle ScholarPubMed
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, 278–298.CrossRefGoogle Scholar
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, 181–200.CrossRefGoogle ScholarPubMed
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, 670–682.CrossRefGoogle ScholarPubMed
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, 438–444.CrossRefGoogle Scholar
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, 235–244.CrossRefGoogle ScholarPubMed
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, 283–297.CrossRefGoogle ScholarPubMed
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.Google Scholar
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, 282–304.CrossRefGoogle Scholar
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, 13–29.CrossRefGoogle ScholarPubMed
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, 1076–1092.CrossRefGoogle ScholarPubMed
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, 8771–8785.CrossRefGoogle ScholarPubMed
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, 9696–9710.CrossRefGoogle ScholarPubMed
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, 233–242.CrossRefGoogle ScholarPubMed
Voogd, J. (1967). Comparative aspects of the structure and fibre connexions of the mammalian cerebellum. Progress in Brain Research 25, 94–134.CrossRefGoogle ScholarPubMed
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. 207–234. New York: Raven Press.Google Scholar
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, 137–151.Google Scholar
Voogd, J. & Glickstein, M. (1998). The anatomy of the cerebellum. Trends in Neurosciences 21, 370–375.CrossRefGoogle ScholarPubMed
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, 4645–4656.CrossRefGoogle ScholarPubMed
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, 5–21.CrossRefGoogle Scholar
Voogd, J. & Wylie, D.R. (2004). Functional and anatomical organization of floccular zones: A preserved feature in vertebrates. The Journal of Comparative Neurology 470, 107–112.CrossRefGoogle ScholarPubMed
Wadiche, J.I. & Jahr, C.E. (2005). Patterned expression of Purkinje cell glutamate transporters controls synaptic plasticity. Nature Neuroscience 8, 1329–1334.CrossRefGoogle ScholarPubMed
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, 37–125.CrossRefGoogle ScholarPubMed
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, 63–78.CrossRefGoogle ScholarPubMed
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, 127–139.CrossRefGoogle Scholar
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, 97–118.3.0.CO;2-O>CrossRefGoogle ScholarPubMed
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, 502–513.3.0.CO;2-E>CrossRefGoogle Scholar
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, 140–153.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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, 2632–2646.CrossRefGoogle ScholarPubMed
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, 97–100.CrossRefGoogle ScholarPubMed