Unipolar brush cell: a potential feedforward excitatory interneuron of the cerebellum

Diño, Maria R.; Schuerger, R.J.; Liu, Y.-B; Slater, N. T.; Mugnaini, Enrico

doi:10.1016/s0306-4522(00)00123-8

Cited by 110 publications

(83 citation statements)

References 20 publications

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“…Unipolar brush cells (UBCs) are found in abundance in the granule cell layer, particularly in the uvula-nodulus (Mugnaini and Floris, 1994;Diño et al, 2000). We recorded from 31 UBCs, identified in the granule cell layer by their larger somata (8 -10 m) and characteristic brush-like endings (Figs.…”

Section: Unipolar Brush Cellsmentioning

confidence: 99%

“…The discharge of UBCs reflects an input mainly from vestibular primary afferent mossy fibers (Rossi et al, 1995;Diño et al, 2000Diño et al, , 2001. UBCs amplify vestibular primary afferent signals and evoke synaptic feedforward excitation of neighboring granule cells.…”

Section: Excitatory Influence Of Ubcs On Granule Cellsmentioning

confidence: 99%

“…Several interneurons synapse on granule cells and/or Purkinje cells and may contribute to the modulation of SSs. Unipolar brush cells (UBCs) amplify vestibular primary afferent mossy fiber projections through synaptic feedforward excitation onto granule cells (Diño et al, 2000;Nunzi et al, 2001). Basket cell inhibitory axon terminals encapsulate Purkinje cell somata (Andersen et al, 1964;Eccles et al, 1965;Fox et al, 1967).…”

Section: Introductionmentioning

confidence: 99%

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Functions of Interneurons in Mouse Cerebellum

Barmack¹,

Yakhnitsa²

2008

J. Neurosci.

217

259

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The output signal of Purkinje cells is conveyed by the modulated discharge of simple spikes (SSs) often ascribed to mossy fiber-granule cell-parallel fiber inputs to Purkinje cell dendrites. Although generally accepted, this view lacks experimental support. We can address this view by controlling afferent signals that reach the cerebellum over climbing and mossy fiber pathways. Vestibular primary afferents constitute the largest mossy fiber projection to the uvula-nodulus. The discharge of vestibular primary afferent mossy fibers increases during ipsilateral roll tilt. The discharge of SSs decreases during ipsilateral roll tilt. Climbing fiber discharge [complex spikes (CSs)] increases during ipsilateral roll tilt. These observations suggest that the modulation of SSs during vestibular stimulation cannot be attributed directly to vestibular mossy fiber afferents. Rather we suggest that interneurons driven by vestibular climbing fibers may determine SS modulation. We recorded from cerebellar interneurons (granule, unipolar brush, Golgi, stellate, basket, and Lugaro cells) and Purkinje cells in the uvula-nodulus of anesthetized mice during vestibular stimulation. We identified all neuronal types by juxtacellular labeling with neurobiotin. Granule, unipolar brush, stellate, and basket cells discharge in phase with ipsilateral roll tilt and in phase with CSs. Golgi cells discharge out of phase with ipsilateral roll tilt and out of phase with CSs. The phases of stellate and basket cell discharge suggests that their activity could account for the antiphasic behavior of CSs and SSs. Because Golgi cells discharge in phase with SSs, Golgi cell activity cannot account for SS modulation. The sagittal array of Golgi cell axon terminals suggests that they contribute to the organization of discrete parasagittal vestibular zones.

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Section: Unipolar Brush Cellsmentioning

confidence: 99%

Section: Excitatory Influence Of Ubcs On Granule Cellsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Functions of Interneurons in Mouse Cerebellum

Barmack¹,

Yakhnitsa²

2008

J. Neurosci.

217

259

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“…Structurally, the synapses in these rosettes appear asymmetric (Berthie and Axelrad 1994;Rossi et al 1995). Unipolar brush cells are glutamatergic (Nunzi et al 2001), and given their wiring, they may contribute to a patterned spread of vestibular aVerent excitation within the granule cell layer that has been considered to be equivalent to a feed-forward excitation (Dino et al 2000). Their primary function seems to be to coordinate the synchronized activity of sets of granule cells, which in turn would regulate activity in spatially restricted subsets of Purkinje cells (cf Nunzi et al 2001 for further details).…”

Section: Unipolar Brush Cellsmentioning

confidence: 99%

Besides Purkinje cells and granule neurons: an appraisal of the cell biology of the interneurons of the cerebellar cortex

Schilling

Oberdick

Rossi

et al. 2008

Histochem Cell Biol

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Ever since the groundbreaking work of Ramon y Cajal, the cerebellar cortex has been recognized as one of the most regularly structured and wired parts of the brain formed by a rather limited set of distinct cells. Its rather protracted course of development, which persists well into postnatal life, the availability of multiple natural mutants, and, more recently, the availability of distinct molecular genetic tools to identify and manipulate discrete cell types have suggested the cerebellar cortex as an excellent model to understand the formation and working of the central nervous system. However, the formulation of a unifying model of cerebellar function has so far proven to be a most cantankerous problem, not least because our understanding of the internal cerebellar cortical circuitry is clearly spotty. Recent research has highlighted the fact that cerebellar cortical interneurons are a quite more diverse and heterogeneous class of cells than generally appreciated, and have provided novel insights into the mechanisms that underpin the development and histogenetic integration of these cells. Here, we provide a short overview of cerebellar cortical interneuron diversity, and we summarize some recent results that are hoped to provide a primer on current understanding of cerebellar biology.

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“…With enough determination and tweaking, we eventually showed that the back-filled rosette-shaped enlargements were the central component of glomeruli where UBC axon terminals formed synapses not only with granule cells but also with other UBCs. Although we were not able to get paired recordings from a UBC and its postsynaptic target, we were able to identify granule cells that responded to white matter stimulation with long-latency repetitive bursts of polysynaptic activity [16].…”

mentioning

confidence: 92%

Commentary on “E. Mugnaini and A. Floris, The Unipolar Brush Cell: A Neglected Neuron of the Mammalian Cerebellar Cortex. J Comp Neurol, 339:174–180, 1994”

2015

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One of the accomplishments of Enrico's laboratory in the late 1980s-then at the University of Connecticut in Storrs-was demonstrating that cerebellar-like neuronal microcircuits exist in the acoustic brainstem [1]. This was done by coupling classic neuroanatomical methods (such as electron microscopy and tract tracing) to what were then two novel techniques: immunocytochemical cell-specific neuronal labeling and the use of transgenic mice. Thus, in the early 1990s, the laboratory focused on clarifying the precise organization, input and output, and evolutionary significance of the recently identified cerebellar-like microcircuit in the mammalian dorsal cochlear nuclear complex (DCN). At the same time, Enrico's laboratory continued its long-standing interest in cerebellar organization and development (Enrico's cerebellar grant was continuously funded for what might be a record-setting 38 years [2]).Like most serendipitous scientific discoveries, the unipolar brush cell's (UBC's) identification was both unforeseen and unplanned, but nevertheless the by-product of a sagacious and prepared mind. Because the Purkinje cell markers used in the DCN studies were mostly calcium-binding proteins (calbindin, PEP-19, and parvalbumin), Enrico constantly reached out to potential collaborators who worked with this family of proteins. Among them was David Jacobowitz from the NIH, who sent us antibodies to the calcium-binding protein calretinin, which turned out to be a cell-marker for what we now know as one of the UBC subtypes [3]. As a beginning graduate student, I had no notion of what we had found. But Enrico immediately put it into context, recalling studies describing novel cerebellar neurons primarily localized to the vestibulocerebellum: Altman and Bayer's pale cells [4], Susan Hockfield's Rat-302 cells [5], Munoz' monodendritic neurons [6], and the secretogranin-positive cells described by Cozzi et al. [7].Bringing to bear his expertise and encyclopedic knowledge of classic neuroanatomy and electron microscopy, Enrico turned his attention to the UBC's ultrastructure and synaptology [8] and quickly realized that previous studies (including his own) had already described UBC features but mistakenly attributed them to other cerebellar cell types. For example, the Bhairy dendrites^and ringlet subunits that he had previously described for Golgi cells of the cat cerebellum [9], and the giant mossy fiber Ben marron^synapse previously described on the postsynaptic Golgi II neuron by ChanPalay and Palay [10]: all of these turned out to be UBC hallmarks. Other telltale features of the UBC revealed by a combination of pre-and post-embedding immunoelectron microscopy included a high density of large dense-cored vesicles; an abundance of high molecular weight neurofilament protein, whose dephosphorylated variant was later identified as the Rat-302 protein [11]; a postsynaptic microfilamentous actin web under the giant mossy fiber-UBC synapse [12]; and the The Introduction article of Cerebellar Classic XI is available at http:// dx

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Unipolar brush cell: a potential feedforward excitatory interneuron of the cerebellum

Cited by 110 publications

References 20 publications

Functions of Interneurons in Mouse Cerebellum

Functions of Interneurons in Mouse Cerebellum

Besides Purkinje cells and granule neurons: an appraisal of the cell biology of the interneurons of the cerebellar cortex

Commentary on “E. Mugnaini and A. Floris, The Unipolar Brush Cell: A Neglected Neuron of the Mammalian Cerebellar Cortex. J Comp Neurol, 339:174–180, 1994”

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