Anatomical investigation of potential contacts between climbing fibers and cerebellar Golgi cells in the mouse

Galliano, Elisa; Baratella, Marco; Sgritta, Martina; Ruigrok, Tom J. H.; Haasdijk, Elize D.; Hoebeek, Freek E.; D’Angelo, Egidio; Jaarsma, Dick; Zeeuw, Chris I. De

doi:10.3389/fncir.2013.00059

Cited by 22 publications

(19 citation statements)

References 32 publications

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“…However, recent immunocytochemical studies, using both pre-and postsynaptic markers, have failed to confirm climbing fiber synapses on Golgi cell dendrites in the molecular layer or on Golgi cell soma in the granule cell layer [19].…”

Section: Dual Afferent Pathways To the Cerebellum And Two Purkinje Cementioning

confidence: 98%

Climbing Fibers Mediate Vestibular Modulation of Both “Complex” and “Simple Spikes” in Purkinje Cells

Barmack

Yakhnitsa

2015

Cerebellum

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Climbing and mossy fibers comprise two distinct afferent paths to the cerebellum. Climbing fibers directly evoke a large multispiked action potential in Purkinje cells termed a "complex spike" (CS). By logical exclusion, the other class of Purkinje cell action potential, termed "simple spike" (SS), has often been attributed to activity conveyed by mossy fibers and relayed to Purkinje cells through granule cells. Here, we investigate the relative importance of climbing and mossy fiber pathways in modulating neuronal activity by recording extracellularly from Purkinje cells, as well as from mossy fiber terminals and interneurons in folia 8-10. Sinusoidal roll-tilt vestibular stimulation vigorously modulates the discharge of climbing and mossy fiber afferents, Purkinje cells, and interneurons in folia 9-10 in anesthetized mice. Roll-tilt onto the side ipsilateral to the recording site increases the discharge of both climbing fibers (CSs) and mossy fibers. However, the discharges of SSs decrease during ipsilateral roll-tilt. Unilateral microlesions of the beta nucleus (β-nucleus) of the inferior olive blocks vestibular modulation of both CSs and SSs in contralateral Purkinje cells. The blockage of SSs occurs even though primary and secondary vestibular mossy fibers remain intact. When mossy fiber afferents are damaged by a unilateral labyrinthectomy (UL), vestibular modulation of SSs in Purkinje cells ipsilateral to the UL remains intact. Two inhibitory interneurons, Golgi and stellate cells, could potentially contribute to climbing fiber-induced modulation of SSs. However, during sinusoidal roll-tilt, only stellate cells discharge appropriately out of phase with the discharge of SSs. Golgi cells discharge in phase with SSs. When the vestibularly modulated discharge is blocked by a microlesion of the inferior olive, the modulated discharge of CSs and SSs is also blocked. When the vestibular mossy fiber pathway is destroyed, vestibular modulation of ipsilateral CSs and SSs persists. We conclude that climbing fibers are primarily responsible for the vestibularly modulated discharge of both CSs and SSs. Modulation of the discharge of SSs is likely caused by climbing fiber-evoked stellate cell inhibition.

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Section: Dual Afferent Pathways To the Cerebellum And Two Purkinje Cementioning

confidence: 98%

Climbing Fibers Mediate Vestibular Modulation of Both “Complex” and “Simple Spikes” in Purkinje Cells

Barmack

Yakhnitsa

2015

Cerebellum

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“…GoCs were visually selected in the cerebellar granular layer by their large soma; the identification of GoCs was confirmed by their passive electrical properties Forti et al, 2006). Pipettes were fabricated with a Sutter P-97 horizontal puller (Sutter Instruments) from thick-walled borosilicate glass capillaries (0.15 mm diameter; Hilgenberg).…”

Section: Electrophysiological Apparatusmentioning

confidence: 99%

“…GrCs undergo inhibitory control by tonic GABA A conductances (Hamann et al, 2002) and by phasic inhibitory synaptic inputs resulting from the spontaneous and evoked discharge of GoCs (Forti et al, 2006;Dugué et al, 2009). Antagonism of inhibitory synaptic currents will thus augment GrC firing upon mf stimulation and preferentially increase the activation of the disynaptic mf-GrC-GoC pathway.…”

Section: Mf and Grc Excitatory Synaptic Inputs Evoked In Golgi Cells mentioning

confidence: 99%

“…In the cerebellar cortex, each of the three glutamatergic elements (mfs, GrCs, and CFs) has a specific phenotype. GrCs express exclusively vGluT1, whereas CFs express vGluT2 only (Fremeau et al, 2001;Hioki et al, 2003). Mossy fibers, depending on their nuclei of origin, can express vGluT1 alone, vGluT2 alone, or both transporters (Fremeau et al, 2001;Hisano et al, 2002;Varoqui et al, 2002;Hioki et al, 2003;Gebre et al, 2012).…”

Section: D-immunohistochemical Quantification Of Ascending Axon Contmentioning

confidence: 99%

“…GrCs express exclusively vGluT1, whereas CFs express vGluT2 only (Fremeau et al, 2001;Hioki et al, 2003). Mossy fibers, depending on their nuclei of origin, can express vGluT1 alone, vGluT2 alone, or both transporters (Fremeau et al, 2001;Hisano et al, 2002;Varoqui et al, 2002;Hioki et al, 2003;Gebre et al, 2012). However, because of the modular organization of the cerebellar cortex, some regions are completely devoid of mfs expressing only vGluT1 (Gebre et al, 2012).…”

Section: D-immunohistochemical Quantification Of Ascending Axon Contmentioning

confidence: 99%

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Granule Cell Ascending Axon Excitatory Synapses onto Golgi Cells Implement a Potent Feedback Circuit in the Cerebellar Granular Layer

Cesana

Pietrajtis

Bidoret

et al. 2013

Journal of Neuroscience

113

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The function of inhibitory interneurons within brain microcircuits depends critically on the nature and properties of their excitatory synaptic drive. Golgi cells (GoCs) of the cerebellum inhibit cerebellar granule cells (GrCs) and are driven both by feedforward mossy fiber (mf) and feedback GrC excitation. Here, we have characterized GrC inputs to GoCs in rats and mice. We show that, during sustained mf discharge, synapses from local GrCs contribute equivalent charge to GoCs as mf synapses, arguing for the importance of the feedback inhibition. Previous studies predicted that GrC-GoC synapses occur predominantly between parallel fibers (pfs) and apical GoC dendrites in the molecular layer (ML). By combining EM and Ca 2ϩ imaging, we now demonstrate the presence of functional synaptic contacts between ascending axons (aa) of GrCs and basolateral dendrites of GoCs in the granular layer (GL). Immunohistochemical quantification estimates these contacts to be ϳ400 per GoC. Using Ca 2ϩ imaging to identify synaptic inputs, we show that EPSCs from aa and mf contacts in basolateral dendrites display similarly fast kinetics, whereas pf inputs in the ML exhibit markedly slower kinetics as they undergo strong filtering by apical dendrites. We estimate that approximately half of the local GrC contacts generate fast EPSCs, indicating their basolateral location in the GL. We conclude that GrCs, through their aa contacts onto proximal GoC dendrites, define a powerful feedback inhibitory circuit in the GL.

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The Mouse Brainstem (Truncus encephali)

Schröder

Moser

Huggenberger

2020

Neuroanatomy of the Mouse

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Anatomical investigation of potential contacts between climbing fibers and cerebellar Golgi cells in the mouse

Cited by 22 publications

References 32 publications

Climbing Fibers Mediate Vestibular Modulation of Both “Complex” and “Simple Spikes” in Purkinje Cells

Climbing Fibers Mediate Vestibular Modulation of Both “Complex” and “Simple Spikes” in Purkinje Cells

Granule Cell Ascending Axon Excitatory Synapses onto Golgi Cells Implement a Potent Feedback Circuit in the Cerebellar Granular Layer

The Mouse Brainstem (Truncus encephali)

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