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Bell Et Al Annual ANRV346-NE31-01 ARI 14 May 2008 6:50 Cerebellum-Like Structures and Their Implications for Cerebellar Function Curtis C. Bell,1 Victor Han,2 and Nathaniel B. Sawtell1 1Neurological Sciences Institute, Oregon Health and Science University, Beaverton, Oregon 97006; email: [email protected], [email protected] 2Oregon Regional Primate Center, Oregon Health and Science University, Beaverton, Oregon 97006; email: [email protected] Annu. Rev. Neurosci. 2008. 31:1–24 Key Words First published online as a Review in Advance on by University of Utah - Marriot Library on 08/20/08. For personal use only. forward model, synaptic plasticity, electric fish, cerebellum February 14, 2008 Annu. Rev. Neurosci. 2008.31:1-24. Downloaded from arjournals.annualreviews.org The Annual Review of Neuroscience is online at Abstract neuro.annualreviews.org The nervous systems of most vertebrates include both the cerebellum This article’s doi: and structures that are architecturally similar to the cerebellum. 10.1146/annurev.neuro.30.051606.094225 The cerebellum-like structures are sensory structures that receive Copyright c 2008 by Annual Reviews. input from the periphery in their deep layers and parallel fiber input All rights reserved in their molecular layers. This review describes these cerebellum- 0147-006X/08/0721-0001$20.00 like structures and compares them with the cerebellum itself. The cerebellum-like structures in three groups of fish act as adaptive sensory processors in which the signals conveyed by parallel fibers in the molecular layer predict the patterns of sensory input to the deep layers through a process of associative synaptic plasticity. Similarities between the cerebellum-like structures and the cerebellum suggest that the cerebellum may also generate predictions about expected sensory inputs or states of the system, as suggested also by clinical, experimental, and theoretical studies of the cerebellum. Understanding the process of predicting sensory patterns in cerebellum-like structures may therefore be a source of insight into cerebellar function. 1 ANRV346-NE31-01 ARI 14 May 2008 6:50 parallel fibers together with the dendrites and Contents cell bodies on which the fibers terminate. The parallel fibers are numerous and closely packed. LOCAL CIRCUITRY, GENE The granule cells that give rise to the paral- EXPRESSION, AND lel fibers in cerebellum-like structures are mor- EVOLUTION OF phologically similar to cerebellar granular cells CEREBELLUM-LIKE (Mugnaini et al. 1980a,b) but are usually located STRUCTURES ................... 2 in an external granule cell mass rather than in General Features................... 2 a granule cell layer beneath the molecular layer Local Circuitry of Different as in the cerebellum. Unipolar brush cells and Cerebellum-Like Structures ..... 3 Golgi cells similar to those present in the gran- Comparison of the Local Circuitries ular layer of the cerebellum are also present of Cerebellum-Like Structures in some cerebellum-like structures (Campbell and the Cerebellum ............. 9 et al. 2007, Mugnaini et al. 1997). Patterns of Gene Expression in Functionally, the parallel fibers convey a rich Cerebellum-Like Structures variety of information from other central struc- and the Cerebellum ............. 10 tures, which includes corollary discharge in- Evolution of Cerebellum-Like formation associated with motor commands, Structures and the Cerebellum . 11 information from higher levels of the same sen- PREDICTIONS AND PLASTICITY sory modality represented in the deep layers, IN CEREBELLUM-LIKE and information from other sensory modalities. STRUCTURES AND THE In general, the types of signals conveyed by par- CEREBELLUM .................. 11 allel fibers are signals that are likely to be asso- Predictions and Plasticity in ciated with changes in the sensory input to the Cerebellum-Like Structures ..... 11 deep layers and that can therefore serve to pre- Predictions in the Cerebellum ...... 15 dict such sensory input (“predictive inputs” in DIRECTIONS FOR FUTURE Figure 1). RESEARCH ...................... 16 The parallel fibers terminate on the den- Activity Patterns in Granule Cells. 16 by University of Utah - Marriot Library on 08/20/08. For personal use only. dritic spines of principal cells and on the smooth Adaptive Filtering in Electrosensory Annu. Rev. Neurosci. 2008.31:1-24. Downloaded from arjournals.annualreviews.org dendrites of inhibitory stellate cells in a man- Systems ........................ 17 ner very similar to the termination of paral- Adaptive Filtering in the DCN lel fibers on Purkinje cells and molecular layer and Less-Studied interneurons of the cerebellum. We use the Cerebellum-Like Structures ..... 17 term principal cells to refer to large cells with Purkinje-Like Cells ................ 17 spine-covered dendrites that extend through- Primitive Cerebellums ............. 17 out the molecular layer. Some of these prin- cipal cells are excitatory efferent cells that project to higher levels of the sensory system, whereas others are inhibitory neurons that ter- LOCAL CIRCUITRY, GENE minate locally on each other and on the effer- EXPRESSION, AND EVOLUTION ent cells. The latter are sometimes referred to OF CEREBELLUM-LIKE as “Purkinje-like.” The cell bodies of principal STRUCTURES cells are usually located in a separate layer be- low the molecular layer, like the Purkinje cell General Features layer of the cerebellum. A distinctive molecular layer is a key identi- Afferent input from the periphery termi- fying feature of all cerebellum-like structures nates in the deep layers of cerebellum-like (Figure 1). The molecular layer is composed of structures, on basilar dendrites of principal 2 Bell · Han · Sawtell ANRV346-NE31-01 ARI 14 May 2008 6:50 Predictive inputs Corollary discharge signals Higher levels of the same modality Other sensory modalities Granule layer (e.g. proprioception) ??? Molecular layer Principal cell layer Sensory input layer Input from a sensory surface Figure 1 Schematic drawing showing major features of cerebellum-like sensory structures. Inhibitory stellate cells of the molecular layer are shown in black. Blue upward arrows indicate afferent input from the periphery terminating in the sensory input layer. In some cerebellum-like structures the afferent input also terminates on the smooth proximal portion of the apical dendrites as indicated by the small blue arrowheads. cells, on proximal apical dendrites of principal This review describes major features of the dif- cells, or on interneurons that relay the informa- ferent cerebellum-like structures of craniates tion from the periphery to the principal cells. but is not exhaustive. Recent reviews (Bell 2002, Some of the interneurons of the deep layers Bell & Maler 2005, Montgomery et al. 1995) are inhibitory, allowing for a change of sign, and the original papers on individual structures, by University of Utah - Marriot Library on 08/20/08. For personal use only. whereby excitation in the periphery is con- as provided below, should be consulted for more Annu. Rev. Neurosci. 2008.31:1-24. Downloaded from arjournals.annualreviews.org verted into inhibition of some principal cells. complete descriptions. Some of the structures The peripheral input to the deep layers forms a are also much better known than others, which map of a sensory surface, such as the skin sur- is reflected in the level of detail in the following face, the retina, or the cochlea. descriptions. Medial octavolateral nucleus. The medial Local Circuitry of Different octavolateral nucleus (MON) processes pri- Cerebellum-Like Structures mary afferent input from the mechanical lateral The brains of all major groups of craniates line system and, in some fish, from eighth nerve except reptiles and birds have cerebellum-like end organs (Bell 1981b, McCormick 1999). It structures (Figures 2 and 3). The similari- is present in all basal aquatic craniates with me- ties among the different cerebellum-like struc- chanical lateral line sensory systems (Figures 2, tures are clear, but so are the differences. Dif- 3a–d, 4a). Myxinoids (atlantic hagfish; C.B. ferent structures may have different types of Braun, personal communication) and aquatic cells in addition to the principal cells, stel- amniotes (reptiles, birds, and mammals; Mont- late cells, and granule cells that are present in gomery et al. 1995) do not have lateral line sys- all cerebellum-like structures. Moreover, some tems and do not have an MON. structures have additional inputs besides the in- The efferent cells of the MON extend their MON: medial octavolateral nucleus puts from the periphery and the parallel fibers. spiny apical dendrites up into a molecular www.annualreviews.org • Cerebellum-Like Structures and Their Implications for Cerebellar Function 3 ANRV346-NE31-01 ARI 14 May 2008 6:50 CBM MON DON OTML ELL RLN DCN Myxinoidea Myxinoids ? Eptatretidae ? Petromyzontiformes Lampetra ? Elasmobranchii Chondrichthyes Holocephalii Chondrosteii Holosteii Neopterygii Osteoglossomorpha a Elopomorpha Teleosteii Clupeomorpha Craniat Vertebrata Euteleostei Actinopterygii Gnathostomata Dipneustii Crossopterygii Urodela Tetrapoda Amphibia Anura Apoda ? ? Sarcopterygii Reptilia Aves Mammalia Figure 2 Distribution of cerebellum-like structures and the cerebellum in different craniate groups. A filled circle means the structure is present by University of Utah - Marriot Library on 08/20/08. For personal use only. in all or almost all the members of that group. A filled half circle means the structure is present only sporadically in that
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