Gene expression profiling of granule cells and Purkinje cells in the zebrafish cerebellum

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The cerebellum is active in some forms of motor learning and coordination and is thought to function in higher cognitive and emotional functions (Ito, 2005). Cerebellar functions rely on neural circuits that are relatively well conserved among vertebrates (Butler and Hodos, 1996). In all vertebrate species, the cerebellum contains similar sets of neurons and glial cells (Butler and Hodos, 1996; Altman and Bayer, 1997). The major glutamatergic excitatory and GABAergic inhibitory neurons in the cerebellum are granule cells and Purkinje cells, respectively. Granule cells, which are derived from neuronal progenitors located in the upper rhombic lip, express the proneural gene atoh1, whereas Purkinje cells, which are derived from neuronal progenitors located in the ventricular zone, express the proneural gene ptf1a (Wingate and Hatten, 1999; Wingate, 2005; Zervas et al., 2004; Hoshino, 2006). Although the two sets of neuronal progenitors are located in adjacent regions of the dorsoanterior hindbrain, they follow distinct genetic programs for their differentiation to granule or Purkinje cells.
Purkinje cells and granule cells receive afferent inputs from outside the cerebellum through climbing fibers and mossy fibers, respectively (Butler and Hodos, 1996; Altman and Bayer, 1997). Climbing fibers, which originate from the inferior olive nucleus (IO) in the caudoventral hindbrain, innervate the dendrites of Purkinje cells. Mossy fibers, which are the axons of neurons in the precerebellar nuclei found in various regions of the brain, form synapses with granule‐cell dendrites. Information is conveyed from the mossy fibers to Purkinje‐cell dendrites by the axons of the granule cells, which are called parallel fibers. Information from mossy fibers and climbing fibers is integrated into the Purkinje cells, which send outputs to projection neurons that extend axons outside the cerebellum. The mammalian cerebellum and the valvula cerebelli and the corpus cerebelli (the anteromedial lobes) of the teleost cerebellum have three layers (Butler and Hodos, 1996; Altman and Bayer, 1997; Bae et al., 2009; Hashimoto and Hibi, 2012; Hibi and Shimizu, 2012). Granule cells are in the deepest layer, called the granule cell layer; Purkinje‐cell somata are in the Purkinje‐cell layer, which is above the granule‐cell layer; and parallel fibers form synapses on the dendrites of Purkinje cells in the superficial layer, called the molecular layer. In addition to the cerebellar neurons, Bergmann glia cell bodies are located near the Purkinje‐cell layer or in the molecular layer and extend glial processes to both the superficial (pial) and the deep (ventricular) sides (Altman and Bayer, 1997; Bae et al., 2009).
Although essential structures of the cerebellum are conserved, comparative anatomical studies have revealed species‐specific features (Butler and Hodos, 1996). In particular, the cerebella of zebrafish and other teleosts have features that are not seen in mammalian cerebella. For example, in the mammalian cerebellum, projection neurons are found in cerebellar nuclei deep inside the brain, whereas, in the teleost cerebellum, the projection neurons (called eurydendroid cells) are located near the Purkinje cells (Nieuwenhuys et al., 1974; Finger, 1978; Pouwels, 1978; Ikenaga et al., 2005; Bae et al., 2009). The origin of projection neurons may also differ between mammals and zebrafish (Kani et al., 2010). Furthermore, the zebrafish caudolateral lobes (the lobus caudalis cerebelli and eminentia granularis) contain only granule cells (Bae et al., 2009). The granule cells in the anteromedial lobes send their axons only to the dendrites of Purkinje cells, whereas granule cells in the caudolateral lobes send axons to the dendrites of Purkinje cells in the cerebellum and additionally extend the axons to the dendrites of crest cells in the crista cerebellaris of the dorsal hindbrain (Bae et al., 2009; Volkmann et al., 2010; Wullimann and Grothe, 2014; Takeuchi et al., 2015b).
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