Functional units of the cerebellum - sagittal zones and microzones

doi:10.1016/0166-2236(79)90057-2

Trends in Neurosciences

Volume 2, 1979, Pages 143-145

https://doi.org/10.1016/0166-2236(79)90057-2 Get rights and content

Abstract

The functional units of the cerebellar cortex have been identified as sagittal zones with a width of about 1 mm and a length of up to more than 100 mm. These zones can be divided into sagittal microzones with a width of 200 μm or less. The microzones and their efferent relay neurones in the cerebellar nuclei might form the operational units of the cerebellum, corresponding in a sense with the classical cell columns of the cerebral cortex.

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Longtemps considéré comme régulateur des seuls mouvements, le cervelet apparaît désormais moduler l’ensemble des activités cognitives et émotionnelles. En particulier, sa région caudale, la plus récente phylogénétiquement, correspondant aux lobules VII et VIII, s’est massivement développée parallèlement aux néocortex associatifs notamment préfrontal, et a été incorporée à de multiples circuits cortico-cérébello-corticales impliqués dans les fonctions non-motrices : exécutives, affectives, attentionnelles, mnésiques et linguistiques. Ainsi coexistent au sein du cortex cérébelleux des régions motrices (lobules I-VI rostral et VIII) avec, majoritairement, des régions cognitives/affectives (lobules VI caudal et VII étendus aux lobules VIII et IX). Les lésions des premières conduisent cliniquement à un syndrome d’ataxie motrice, tandis-que les lésions des secondes entraînent l’émergence de dysfonctionnements cognitifs et émotionnels. De plus, ces symptômes peuvent se retrouver au sein de troubles psychiatriques ou neurodéveloppementaux pour lesquels des atteintes du cervelet ont été rapportées. Enfin, en raison de son homogénéité structurale, il est postulé que le cervelet doit accomplir la même fonction que ce soit pour la motricité ou pour la cognition. Le cervelet jouerait ainsi un rôle de modulateur général contrôlant, rectifiant, optimisant et automatisant les opérations cérébrales dont le domaine fonctionnel dépendrait de la spécificité des connections cérébello-corticales. En d’autres termes, une révolution conceptuelle concernant le cervelet s’est opérée en une trentaine d’années. Nous nous proposons dans cet article de présenter les principales données récentes tant cliniques qu’issues de l’imagerie cérébrale morphologique et fonctionnelle, qui ont contraint de redéfinir le rôle du cervelet et d’en élargir la sphère d’influence.
Although the cerebellum was thought to be devoted exclusively to movement regulation and learning, it now appears to be implicated in cognition and emotion. In particular, its caudal and more phylogenetically recent region, corresponding to lobules VII and VIII, strongly developped in parallel with the associative neocortex, especially prefrontal, and has been integrated in multiple cortico-cerebello-cortical loops involved, at least, in: executive, affective, attentional, mnesic and linguistic functions. The cerebellar cortex encompasses motor territories (lobules I-VI rostral and VIII) and, mostly, cognitive/affective territories (lobules VI caudal and VII extended to lobules VIII and IX). Lesions of the motor cerebellum cause motor ataxia, whereas lesions of the remaining cerebellum induce cognitive and emotional impairments. Moreover, these deficits can be included in clinical presentation of several neurodevelopmental and psychiatric diseases associated with cerebellar structural and functional alterations. Finally, because of its regular structure, the cerebellum is assumed to perform the same computation in the motor domain as well as in the cognitive/affective one. The cerebellum would play a general modulatory role allowing correction, optimization and automation of cerebral operations, whose specific functional domain would depend upon its connectivity. Therefore, in thirty years, « a conceptual revolution » has occurred in the functional approaches of the cerebellum. In the current brief review, we will present the main data arising from clinical, structural and functional neuroimaging studies, which contributed to broaden the function of the cerebellum from movement to cognition and emotion.
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Citation Excerpt :
Climbing fibres from different sub-nuclei of the inferior olive terminate in discrete, rostral-caudal zones (Fig. 1B)1. The zones are further subdivided into microzones that are innervated by subsets of CFs with similar response properties that relate to the sensory inputs of their olivary source neurons (Andersson and Oscarsson, 1978; Ekerot and Larson, 1979a, 1979b; Oscarsson, 1979; Voogd and Bigare, 1980; Buisseret-Delmas and Angaut, 1993; Garwicz and Ekerot, 1994; Hesslow, 1994a, 1994b; Sugihara and Shinoda, 2004). Mossy fibres terminate on granule cells, the axons of which ascend to the molecular layer, bifurcate and extend several millimetres medio-laterally as parallel fibres (PFs) (Napper and Harvey, 1988; Pichitpornchai et al., 1994; Coutinho et al., 2004).
The geometry of the glutamatergic mossy-parallel fibre and climbing fibre inputs to cerebellar cortical Purkinje cells has powerfully influenced thinking about cerebellar functions. The compartmentation of the cerebellum into parasagittal zones, identifiable in olivo-cortico-nuclear projections, and the trajectories of the parallel fibres, transverse to these zones and following the long axes of the cortical folia, are particularly important. Two monoaminergic afferent systems, the serotonergic and noradrenergic, are major inputs to the cerebellar cortex but their architecture and relationship with the cortical geometry are poorly understood. Immunohistochemistry for the serotonin transporter (SERT) and for the noradrenaline transporter (NET) revealed strong anisotropy of these afferent fibres in the molecular layer of rat cerebellar cortex. Individual serotonergic fibres travel predominantly medial–lateral, along the long axes of the cortical folia, similar to parallel fibres and Zebrin II immunohistochemistry revealed that they can influence multiple zones. In contrast, individual noradrenergic fibres run predominantly parasagittally with rostral-caudal extents significantly longer than their medial–lateral deviations. Their local area of influence has similarities in form and size to those of identified microzones. Within the molecular layer, the orthogonal trajectories of these two afferent systems suggest different information processing. An individual serotonergic fibre must influence all zones and microzones within its medial–lateral trajectory. In contrast, noradrenergic fibres can influence smaller cortical territories, potentially as limited as a microzone. Evidence is emerging that these monoaminergic systems may not supply a global signal to all of their targets and their potential for cerebellar cortical functions is discussed.
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2021, Neuroscience
This article is dedicated to the memory of Masao Ito. Masao Ito made numerous important contributions revealing the function of the cerebellum in motor control. His pioneering contributions to cerebellar physiology began with his discovery of inhibition and disinhibition of target neurons by cerebellar Purkinje cells, and his discovery of the presence of long-term depression in parallel fiber–Purkinje cell synapses. Purkinje cells formed the nodal point of Masao Ito’s landmark model of motor control by the cerebellum. These discoveries became the basis for his ideas regarding the flocculus hypothesis, the adaptive motor control system, and motor learning by the cerebellum, inspiring many new experiments to test his hypotheses. This article will trace the achievements of Ito and colleagues in analyzing the neural circuits of the input–output organization of the cerebellar cortex and nuclei, particularly with respect to motor control. The article will discuss some of the important issues that have been solved and also those that remain to be solved for our understanding of motor control by the cerebellum.
Ocular Reflex Adaptation as an Experimental Model of Cerebellar Learning –– In Memory of Masao Ito ––
2021, Neuroscience
Citation Excerpt :
As shown in Fig. 1, HVOR is driven by not only the three-neuron arc of the vestibular nerve, vestibular nuclear (VN) neurons, and extraocular muscle motor neurons, but also the cerebellar FL. The H-zone, a microzone (Oscarsson, 1979; Ito, 1984; Sugihara and Shinoda, 2004) specifically involved in horizontal ocular reflexes, is located in the middle FL (Yamamoto and Shimoyama, 1977; Nagao et al., 1985). The H-zone is identified by the effects of microstimulation, which induce a slow abduction in the ipsilateral eye (Dufossé et al., 1977; Nagao, et al., 1985).
Masao Ito proposed a cerebellar learning hypothesis with Marr and Albus in the early 1970s. He suggested that cerebellar flocculus (FL) Purkinje cells (PCs), which directly inhibit the vestibular nuclear neurons driving extraocular muscle motor neurons, adaptively control the horizontal vestibulo-ocular reflex (HVOR) through the modification of mossy and parallel fiber-mediated vestibular responsiveness by visual climbing fiber (CF) inputs. Later, it was suggested that the same FL PCs adaptively control the horizontal optokinetic response (HOKR) in the same manner through the modification of optokinetic responsiveness in rodents and rabbits. In 1982, Ito and his colleagues discovered the plasticity of long-term depression (LTD) at parallel fiber (PF)–PC synapses after conjunctive stimulation of mossy or parallel fibers with CFs. Long-term potentiation (LTP) at PF–PC synapses by weak PF stimulation alone was found later. Many lines of experimental evidence have supported their hypothesis using various experimental methods and materials for the past 50 years by many research groups. Although several controversial findings were presented regarding their hypothesis, the reasons underlying many of them were clarified. Today, their hypothesis is considered as a fundamental mechanism of cerebellar learning. Furthermore, it was found that the memory of adaptation is transferred from the FL to vestibular nuclei for consolidation by repetition of adaptation through the plasticity of vestibular nuclear neurons. In this article, after overviewing their cerebellar learning hypothesis, I discuss possible roles of LTD and LTP in gain-up and gain-down HVOR/HOKR adaptations and refer to the expansion of their hypothesis to cognitive functions.
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Dexterous forelimb movements like reaching, grasping, and manipulating objects are fundamental building blocks of the mammalian motor repertoire. These behaviors are essential to everyday activities, and their elaboration underlies incredible accomplishments by human beings in art and sport. Moreover, the susceptibility of these behaviors to damage and disease of the nervous system can lead to debilitating deficits, highlighting a need for a better understanding of function and dysfunction in sensorimotor control. The cerebellum is central to coordinating limb movements, as defined in large part by Joseph Babinski and Gordon Holmes describing motor impairment in patients with cerebellar lesions over 100 years ago (Babinski, 1902; Holmes, 1917), and supported by many important human and animal studies that have been conducted since. Here, with a focus on output pathways of the cerebellar nuclei across mammalian species, we describe forelimb movement deficits observed when cerebellar circuits are perturbed, the mechanisms through which these circuits influence motor output, and key challenges in defining how the cerebellum refines limb movement.

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^∗: O. Oscarsson is Professor of Physiology at the Institute of Physiology, University of Lund, Sölvegatan 19, S-223 62 Lund, Sweden.

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Trends in Neurosciences

General reviewFunctional units of the cerebellum - sagittal zones and microzones

Abstract

Brain Res.

Exp. Brain Res.

J. Comp. Neurol.

The Cerebellum as a Neuronal Machine

J. Comp. Neurol.

General review
Functional units of the cerebellum - sagittal zones and microzones