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Article ; Online: Olov Oscarsson's Description of Afferent Pathways to the Cerebellum: Excellent Physiology, Base for Anatomy, and Road Toward Understanding Function.

Ruigrok, Tom J H

2023 Volume 23, Issue 2, Page(s) 284–328

Abstract: Olov Oscarsson's review on the functional organization of spinocerebellar paths is a prime demonstration of the great skills and huge knowledge base of the electrophysiologists of his era working on communication systems in the brain. Oscarsson describes ...

Abstract	Olov Oscarsson's review on the functional organization of spinocerebellar paths is a prime demonstration of the great skills and huge knowledge base of the electrophysiologists of his era working on communication systems in the brain. Oscarsson describes and characterizes in detail no less than ten different communication lines between the spinal cord and the cerebellum. As such, his work proved to be a highly fertile basis for ongoing physiological and anatomical research. However, even after 50 years of continuing cerebellar research, many questions are still open and even care must be taken that the differentiation in spinocerebellar paths, so carefully demonstrated by Oscarsson, is not lost in present-day research.
MeSH term(s)	Neural Pathways/anatomy & histology ; Cerebellum/physiology ; Afferent Pathways ; Olivary Nucleus/physiology ; Purkinje Cells/physiology
Language	English
Publishing date	2023-01-24
Publishing country	United States
Document type	Journal Article
ZDB-ID	2112586-7
ISSN	1473-4230 ; 1473-4222
ISSN (online)	1473-4230
ISSN	1473-4222
DOI	10.1007/s12311-023-01516-6
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Article: A disynaptic basal ganglia connection to the inferior olive: potential for basal ganglia influence on cerebellar learning.

Ruigrok, Tom J H / Wang, Xiaolu / Sabel-Goedknegt, Erika / Coulon, Patrice / Gao, Zhenyu

Frontiers in systems neuroscience

2023 Volume 17, Page(s) 1176126

Abstract: Recent studies have shown that the cerebellum and the basal ganglia are interconnected at subcortical levels. However, a subcortical basal ganglia connection to the inferior olive (IO), being the source of the olivocerebellar climbing fiber system, is ... ...

Abstract	Recent studies have shown that the cerebellum and the basal ganglia are interconnected at subcortical levels. However, a subcortical basal ganglia connection to the inferior olive (IO), being the source of the olivocerebellar climbing fiber system, is not known. We have used classical tracing with CTb, retrograde transneuronal infection with wildtype rabies virus, conditional tracing with genetically modified rabies virus, and examination of material made available by the Allen Brain Institute, to study potential basal ganglia connections to the inferior olive in rats and mice. We show in both species that parvalbumin-positive, and therefore GABAergic, neurons in the entopeduncular nucleus, representing the rodent equivalent of the internal part of the globus pallidus, innervate a group of cells that surrounds the fasciculus retroflexus and that are collectively known as the area parafascicularis prerubralis. As these neurons supply a direct excitatory input to large parts of the inferior olivary complex, we propose that the entopeduncular nucleus, as a main output station of the basal ganglia, provides an inhibitory influence on olivary excitability. As such, this connection may influence olivary involvement in cerebellar learning and/or could be involved in transmission of reward properties that have recently been established for olivocerebellar signaling.
Language	English
Publishing date	2023-05-05
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2453005-0
ISSN	1662-5137
ISSN	1662-5137
DOI	10.3389/fnsys.2023.1176126
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Article: Sympathetic components in left and right human cervical vagus nerve: implications for vagus nerve stimulation.

Ruigrok, Tom J H / Mantel, Sophia A / Orlandini, Lara / de Knegt, Corné / Vincent, Arnaud J P E / Spoor, Jochem K H

Frontiers in neuroanatomy

2023 Volume 17, Page(s) 1205660

Abstract: Cervical vagus nerve stimulation is in a great variety of clinical situations indicated as a form of treatment. It is textbook knowledge that at the cervical level the vagus nerve contains many different fiber classes. Yet, recently, several reports have ...

Abstract	Cervical vagus nerve stimulation is in a great variety of clinical situations indicated as a form of treatment. It is textbook knowledge that at the cervical level the vagus nerve contains many different fiber classes. Yet, recently, several reports have shown that this nerve also may contain an additional class of potentially noradrenergic fibers, suggested to denote efferent sympathetic fibers. As such, the nature and presence of these fibers should be considered when choosing a stimulation protocol. We have studied human vagus material extracted from dissection room cadavers in order to further confirm the presence of this class of fibers, to study their origin and direction within the nerve and to determine their distribution and variability between subjects and pairs of left and right nerves of the same individual. Sections were studied with immunohistochemical techniques using antibodies against tyrosine hydroxylase (TH: presumed to indicate noradrenergic fibers), myelin basic protein and neurofilament. Our results show that at least part of the TH-positive fibers derive from the superior cervical ganglion or sympathetic trunk, do not follow a cranial but take a peripheral course through the nerve. The portion of TH-positive fibers is highly variable between individuals but also between the left and right pairs of the same individual. TH-positive fibers can distribute and wander throughout the fascicles but maintain a generally clustered appearance. The fraction of TH-positive fibers generally diminishes in the left cervical vagus nerve when moving in a caudal direction but remains more constant in the right nerve. These results may help to determine optimal stimulation parameters for cervical vagus stimulation in clinical settings.
Language	English
Publishing date	2023-07-10
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2452969-2
ISSN	1662-5129
ISSN	1662-5129
DOI	10.3389/fnana.2023.1205660
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Article ; Online: Input and output organization of the mesodiencephalic junction for cerebro-cerebellar communication.

Wang, Xiaolu / Novello, Manuele / Gao, Zhenyu / Ruigrok, Tom J H / De Zeeuw, Chris I

Journal of neuroscience research

2021 Volume 100, Issue 2, Page(s) 620–637

Abstract: Most studies investigating the impact of the cerebral cortex (CC) onto the cerebellum highlight the role of the pons, which provides the mossy fibers to the cerebellum. However, cerebro-cerebellar communication may also be mediated by the nuclei of the ... ...

Abstract	Most studies investigating the impact of the cerebral cortex (CC) onto the cerebellum highlight the role of the pons, which provides the mossy fibers to the cerebellum. However, cerebro-cerebellar communication may also be mediated by the nuclei of the mesodiencephalic junction (MDJ) that project to the inferior olive (IO), which in turn provides the climbing fibers to the molecular layer. Here, we uncover the precise topographic relations of the inputs and outputs of the MDJ using multiple, classical, and transneuronal tracing methods as well as analyses of mesoscale cortical injections from Allen Mouse Brain. We show that the caudal parts of the CC predominantly project to the principal olive via the rostral MDJ and that the rostral parts of the CC predominantly project to the rostral medial accessory olive via the caudal MDJ. Moreover, using triple viral tracing technology, we show that the cerebellar nuclei directly innervate the neurons in the MDJ that receive input from CC and project to the IO. By unraveling these topographic and prominent, mono- and disynaptic projections through the MDJ, this work establishes that cerebro-cerebellar communication is not only mediated by the pontine mossy fiber system, but also by the climbing fiber system.
MeSH term(s)	Animals ; Cerebellar Nuclei/physiology ; Cerebellum/physiology ; Medulla Oblongata ; Mice ; Neural Pathways/physiology ; Neurons/physiology ; Olivary Nucleus/physiology
Language	English
Publishing date	2021-12-01
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	195324-2
ISSN	1097-4547 ; 0360-4012
ISSN (online)	1097-4547
ISSN	0360-4012
DOI	10.1002/jnr.24993
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Article ; Online: Cerebellum Lecture: the Cerebellar Nuclei-Core of the Cerebellum.

Kebschull, Justus M / Casoni, Filippo / Consalez, G Giacomo / Goldowitz, Daniel / Hawkes, Richard / Ruigrok, Tom J H / Schilling, Karl / Wingate, Richard / Wu, Joshua / Yeung, Joanna / Uusisaari, Marylka Yoe

Cerebellum (London, England)

2023 Volume 23, Issue 2, Page(s) 620–677

Abstract: The cerebellum is a key player in many brain functions and a major topic of neuroscience research. However, the cerebellar nuclei (CN), the main output structures of the cerebellum, are often overlooked. This neglect is because research on the cerebellum ...

Abstract	The cerebellum is a key player in many brain functions and a major topic of neuroscience research. However, the cerebellar nuclei (CN), the main output structures of the cerebellum, are often overlooked. This neglect is because research on the cerebellum typically focuses on the cortex and tends to treat the CN as relatively simple output nuclei conveying an inverted signal from the cerebellar cortex to the rest of the brain. In this review, by adopting a nucleocentric perspective we aim to rectify this impression. First, we describe CN anatomy and modularity and comprehensively integrate CN architecture with its highly organized but complex afferent and efferent connectivity. This is followed by a novel classification of the specific neuronal classes the CN comprise and speculate on the implications of CN structure and physiology for our understanding of adult cerebellar function. Based on this thorough review of the adult literature we provide a comprehensive overview of CN embryonic development and, by comparing cerebellar structures in various chordate clades, propose an interpretation of CN evolution. Despite their critical importance in cerebellar function, from a clinical perspective intriguingly few, if any, neurological disorders appear to primarily affect the CN. To highlight this curious anomaly, and encourage future nucleocentric interpretations, we build on our review to provide a brief overview of the various syndromes in which the CN are currently implicated. Finally, we summarize the specific perspectives that a nucleocentric view of the cerebellum brings, move major outstanding issues in CN biology to the limelight, and provide a roadmap to the key questions that need to be answered in order to create a comprehensive integrated model of CN structure, function, development, and evolution.
MeSH term(s)	Cerebellar Nuclei/diagnostic imaging ; Cerebellar Nuclei/physiology ; Cerebellum/physiology ; Neurons/physiology
Language	English
Publishing date	2023-02-13
Publishing country	United States
Document type	Journal Article ; Review
ZDB-ID	2112586-7
ISSN	1473-4230 ; 1473-4222
ISSN (online)	1473-4230
ISSN	1473-4222
DOI	10.1007/s12311-022-01506-0
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Article ; Online: Multizonal Cerebellar Influence Over Sensorimotor Areas of the Rat Cerebral Cortex.

Aoki, Sho / Coulon, Patrice / Ruigrok, Tom J H

Cerebral cortex (New York, N.Y. : 1991)

2017 Volume 29, Issue 2, Page(s) 598–614

Abstract: ... time of 66-70 h allowed for third-order retrograde RABV infection of Purkinje cells. CTb served ...

Abstract	The cerebral cortex requires cerebellar input for optimizing sensorimotor processing. However, how the sensorimotor cortex uses cerebellar information is far from understood. One critical and unanswered question is how cerebellar functional entities (zones or modules) are connected to distinct parts of the sensorimotor cortices. Here, we utilized retrograde transneuronal infection of rabies virus (RABV) to study the organization of connections from the cerebellar cortex to M1, M2, and S1 of the rat cerebral cortex. RABV was co-injected with cholera toxin β-subunit (CTb) into each of these cortical regions and a survival time of 66-70 h allowed for third-order retrograde RABV infection of Purkinje cells. CTb served to identify the injection site. RABV+ Purkinje cells throughout cerebellar zones were identified by reference to the cerebellar zebrin pattern. All injections, including those into S1, resulted in multiple, zonally arranged, strips of RABV+ Purkinje cells. M1 injections were characterized by input from Purkinje cells in the vermal X-zone, medial paravermis (C1- and Cx-zones), and lateral hemisphere (D2-zone); M2 receives input from D2- and C3-zones; connections to S1 originate from X-, Cx-, C3-, and D2-zones. We hypothesize that individual domains of the sensorimotor cortex require information from a specific combination of cerebellar modules.
MeSH term(s)	Animals ; Brain Mapping/methods ; Cerebellar Cortex/chemistry ; Cerebellar Cortex/physiology ; Cerebellum/chemistry ; Cerebellum/physiology ; Cerebral Cortex/chemistry ; Cerebral Cortex/physiology ; Male ; Motor Cortex/chemistry ; Motor Cortex/physiology ; Neural Pathways/chemistry ; Neural Pathways/physiology ; Purkinje Cells/chemistry ; Purkinje Cells/physiology ; Rabies virus ; Rats ; Rats, Wistar ; Sensorimotor Cortex/chemistry ; Sensorimotor Cortex/physiology
Language	English
Publishing date	2017-12-30
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1077450-6
ISSN	1460-2199 ; 1047-3211
ISSN (online)	1460-2199
ISSN	1047-3211
DOI	10.1093/cercor/bhx343
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Article: Disynaptic Subthalamic Input to the Posterior Cerebellum in Rat.

Jwair, Saad / Coulon, Patrice / Ruigrok, Tom J H

Frontiers in neuroanatomy

2017 Volume 11, Page(s) 13

Abstract: In the last decade, the interplay between basal ganglia and cerebellar functions has been increasingly advocated to explain their joint operation in both normal and pathological conditions. Yet, insight into the neuroanatomical basis of this interplay ... ...

Abstract	In the last decade, the interplay between basal ganglia and cerebellar functions has been increasingly advocated to explain their joint operation in both normal and pathological conditions. Yet, insight into the neuroanatomical basis of this interplay between both subcortical structures remains sparse and is mainly derived from work in primates. Here, in rodents, we have studied the existence of a potential disynaptic connection between the subthalamic nucleus (STN) and the cerebellar cortex as has been demonstrated earlier for the primate. A mixture of unmodified rabies virus (RABV: CVS 11) and cholera toxin B-subunit (CTb) was injected at places in the posterior cerebellar cortex of nine rats. The survival time was chosen to allow for disynaptic retrograde transneuronal infection of RABV. We examined the STN for neurons infected with RABV in all nine cases and related the results with the location of the RABV/CTb injection site, which ranged from the vermis of lobule VII, to the paravermis and hemispheres of the paramedian lobule and crus 2a. We found that cases with injection sites in the vermis of lobule VII showed prominent RABV labeling in the STN. In contrast, almost no subthalamic labeling was noted in cases with paravermal or hemispheral injection sites. We show circumstantial evidence that not only the pontine nuclei but also the pedunculotegmental nucleus may act as the intermediary in the connection from STN to cerebellar cortex. This finding implies that in the rat the STN links disynaptically to the vermal part of lobule VII of the cerebellar cortex, without any major involvement of the cerebellar areas that are linked to sensorimotor functions. As vermal lobule VII recently has been shown to process disynaptic input from the retrosplenial and orbitofrontal cortices, we hypothesize that in the rat the subthalamic input to cerebellar function might be used to influence more prominently non-motor functions of the cerebellum than motor functions. This latter aspect seems to contradict the primate results and could point to a more elaborate interaction between basal ganglia and cerebellum in more demanding motor tasks.
Language	English
Publishing date	2017-02-28
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2452969-2
ISSN	1662-5129
ISSN	1662-5129
DOI	10.3389/fnana.2017.00013
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Article ; Online: Ins and outs of cerebellar modules.

Ruigrok, Tom J H

Cerebellum (London, England)

2010 Volume 10, Issue 3, Page(s) 464–474

Abstract: The modular concept of cerebellar connections has been advocated in the lifetime work of Jan Voogd. In this concept, a cerebellar module is defined as the conglomerate of one or multiple and non-adjacent, parasagittally arranged zones of Purkinje cells, ... ...

Abstract	The modular concept of cerebellar connections has been advocated in the lifetime work of Jan Voogd. In this concept, a cerebellar module is defined as the conglomerate of one or multiple and non-adjacent, parasagittally arranged zones of Purkinje cells, their specific projection to a well-defined region of the cerebellar nuclei, and the climbing fiber input to these zones by a well-defined region of the inferior olivary complex. The modular organization of these olivo-cortico-nuclear connections is further exemplified by matching reciprocal connections between inferior olive and cerebellar nuclei. Because the different regions of the cerebellar nuclei show highly specific output patterns, cerebellar modules have been suggested to constitute functional entities. This idea is strengthened by the observation that anatomically defined modules adhere to the distribution of chemical markers in the cerebellar cortex suggesting that modules not only differ in their input and output relations but also may differ in operational capabilities. Here, I will briefly review some recent data on the establishment of cerebellar modules in rats. Furthermore, some evidence will be shown suggesting that the other main afferent system (i.e., mossy fibers), at least to some extent, also adheres to the modular organization. Finally, using retrograde transneuronal tracing with rabies virus, some evidence will be provided that several cerebellar modules may be involved in the control of individual muscles.
MeSH term(s)	Animals ; Animals, Newborn ; Brain Mapping ; Cerebellar Cortex/physiology ; Cerebellar Nuclei/physiology ; Male ; Mice ; Mice, Inbred C57BL ; Models, Anatomic ; Muscle, Skeletal/physiology ; Neural Pathways/physiology ; Purkinje Cells/physiology ; Rats ; Rats, Wistar
Language	English
Publishing date	2010-03-16
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2112586-7
ISSN	1473-4230 ; 1473-4222
ISSN (online)	1473-4230
ISSN	1473-4222
DOI	10.1007/s12311-010-0164-y
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Zs.A 5795: Show issues

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Article ; Online: Caveats in Transneuronal Tracing with Unmodified Rabies Virus: An Evaluation of Aberrant Results Using a Nearly Perfect Tracing Technique.

Ruigrok, Tom J H / van Touw, Sven / Coulon, Patrice

Frontiers in neural circuits

2016 Volume 10, Page(s) 46

Abstract: Apart from the genetically engineered, modified, strains of rabies virus (RABV), unmodified 'fixed' virus strains of RABV, such as the 'French' subtype of CVS11, are used to examine synaptically connected networks in the brain. This technique has been ... ...

Abstract	Apart from the genetically engineered, modified, strains of rabies virus (RABV), unmodified 'fixed' virus strains of RABV, such as the 'French' subtype of CVS11, are used to examine synaptically connected networks in the brain. This technique has been shown to have all the prerequisite characteristics for ideal tracing as it does not metabolically affect infected neurons within the time span of the experiment, it is transferred transneuronally in one direction only and to all types of neurons presynaptic to the infected neuron, number of transneuronal steps can be precisely controlled by survival time and it is easily detectable with a sensitive technique. Here, using the 'French' CVS 11 subtype of RABV in Wistar rats, we show that some of these characteristics may not be as perfect as previously indicated. Using injection of RABV in hind limb muscles, we show that RABV-infected spinal motoneurons may already show lysis 1 or 2 days after infection. Using longer survival times we were able to establish that Purkinje cells may succumb approximately 3 days after infection. In addition, some neurons seem to resist infection, as we noted that the number of RABV-infected inferior olivary neurons did not progress in the same rate as other infected neurons. Furthermore, in our hands, we noted that infection of Purkinje cells did not result in expected transneuronal labeling of cell types that are presynaptic to Purkinje cells such as molecular layer interneurons and granule cells. However, these cell types were readily infected when RABV was injected directly in the cerebellar cortex. Conversely, neurons in the cerebellar nuclei that project to the inferior olive did not take up RABV when this was injected in the inferior olive, whereas these cells could be infected with RABV via a transneuronal route. These results suggest that viral entry from the extracellular space depends on other factors or mechanisms than those used for retrograde transneuronal transfer. We conclude that transneuronal tracing with RABV may result in unexpected results, as not all properties of RABV seem to be ubiquitously valid.
MeSH term(s)	Afferent Pathways/virology ; Animals ; Cerebellar Cortex/virology ; Cerebellar Nuclei/virology ; Lower Extremity ; Male ; Motor Neurons/virology ; Muscle, Skeletal/virology ; Nerve Net/virology ; Neuroanatomical Tract-Tracing Techniques/methods ; Olivary Nucleus/virology ; Purkinje Cells/virology ; Rabies ; Rabies virus ; Rats ; Rats, Wistar
Language	English
Publishing date	2016
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2452968-0
ISSN	1662-5110 ; 1662-5110
ISSN (online)	1662-5110
ISSN	1662-5110
DOI	10.3389/fncir.2016.00046
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Article: Collateralization of cerebellar output to functionally distinct brainstem areas. A retrograde, non-fluorescent tracing study in the rat.

Ruigrok, Tom J H / Teune, Thea M

Frontiers in systems neuroscience

2014 Volume 8, Page(s) 23

Abstract: The organization of the cerebellum is characterized by a number of longitudinally organized connection patterns that consist of matching olivo-cortico-nuclear zones. These entities, referred to as modules, have been suggested to act as functional units. ... ...

Abstract	The organization of the cerebellum is characterized by a number of longitudinally organized connection patterns that consist of matching olivo-cortico-nuclear zones. These entities, referred to as modules, have been suggested to act as functional units. The various parts of the cerebellar nuclei (CN) constitute the output of these modules. We have studied to what extent divergent and convergent patterns in the output of the modules to four, functionally distinct brain areas can be recognized. Two retrograde tracers were injected in various combinations of the following nuclei: the red nucleus (RN), as a main premotor nucleus; the prerubral area, as a main supplier of afferents to the inferior olive (IO); the nucleus reticularis tegmenti pontis (NRTP), as a main source of cerebellar mossy fibers; and the IO, as the source of climbing fibers. For all six potential combinations three cases were examined. All nine cases with combinations that involved the IO did not, or hardly, resulted in double labeled neurons. In contrast, all other combinations resulted in at least 10% and up to 67% of double labeled neurons in cerebellar nuclear areas where both tracers were found. These results show that the cerebellar nuclear neurons that terminate within the studied areas represent basically two intermingled populations of projection cells. One population corresponds to the small nucleo-olivary neurons whereas the other consists of medium- to large-sized neurons which are likely to distribute their axons to several other areas. Despite some consistent differences between the output patterns of individual modules we propose that modular cerebellar output to premotor areas such as the RN provides simultaneous feedback to both the mossy fiber and the climbing fiber system and acts in concert with a designated GABAergic nucleo-olivary circuit. These features seem to form a basic characteristic of cerebellar operation.
Language	English
Publishing date	2014-02-21
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2453005-0
ISSN	1662-5137
ISSN	1662-5137
DOI	10.3389/fnsys.2014.00023
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