Purkinje Cells in Posterior Cerebellar Vermis Encode Motion in an Inertial Reference Frame

Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, MO 63110, USA.
Neuron (Impact Factor: 15.05). 07/2007; 54(6):973-85. DOI: 10.1016/j.neuron.2007.06.003
Source: PubMed


The ability to orient and navigate through the terrestrial environment represents a computational challenge common to all vertebrates. It arises because motion sensors in the inner ear, the otolith organs, and the semicircular canals transduce self-motion in an egocentric reference frame. As a result, vestibular afferent information reaching the brain is inappropriate for coding our own motion and orientation relative to the outside world. Here we show that cerebellar cortical neuron activity in vermal lobules 9 and 10 reflects the critical computations of transforming head-centered vestibular afferent information into earth-referenced self-motion and spatial orientation signals. Unlike vestibular and deep cerebellar nuclei neurons, where a mixture of responses was observed, Purkinje cells represent a homogeneous population that encodes inertial motion. They carry the earth-horizontal component of a spatially transformed and temporally integrated rotation signal from the semicircular canals, which is critical for computing head attitude, thus isolating inertial linear accelerations during navigation.

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    • "It therefore crucially monitors sensory information for updating mental representation of space (Rondi-Reig et al., 2014; Lefort et al., 2015). The cerebellum normally uses otolith and semicircular canal signals to convert vestibular head centered into earth-referenced self-motion and spatial orientation signals (Yakusheva et al., 2007). During locomotion-dependent real navigation self-motion information can be used for building and updating spatial representation. "
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    ABSTRACT: Spatial orientation and navigation depends on information from the vestibular system. Previous work suggested impaired spatial navigation in patients with bilateral vestibular failure (BVF). The aim of this study was to investigate event-related brain activity (fMRI) during spatial navigation and visual memory tasks in BVF patients. Twenty-three BVF patients and healthy age-and gender matched control subjects performed learning sessions of spatial navigation by watching short films taking them through various streets from a driver's perspective along a route to the Cathedral of Cologne using virtual reality videos (adopted and modified from Google Earth(®)). In the MRI scanner, participants were asked to respond to questions testing for visual memory or spatial navigation while they viewed short video clips. From a similar but not identical perspective depicted video frames of routes were displayed which they had previously seen or which were completely novel to them. Compared with controls, posterior cerebellar activity in BVF patients was higher during spatial navigation than during visual memory tasks, in the absence of performance differences. This cerebellar activity correlated with disease duration. Cerebellar activity during spatial navigation in BVF patients may reflect increased non-vestibular efforts to counteract the development of spatial navigation deficits in BVF. Conceivably, cerebellar activity indicates a change in navigational strategy of BVF patients, i.e. from a more allocentric, landmark or place -based strategy (hippocampus) to a more sequence-based strategy. This interpretation would be in accord with recent evidence for a cerebellar role in sequence-based navigation. Copyright © 2015. Published by Elsevier Ltd.
    Neuroscience 08/2015; 305. DOI:10.1016/j.neuroscience.2015.07.089 · 3.36 Impact Factor
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    • "Using transgenic L7PKCI mice, which selectively lack protein kinase C-dependent plasticity at parallel fiber-Purkinje cell synapses in the cerebellum, Rochefort et al. (2011) examined hippocampal place cells during navigation. Purkinje cells are thought to transform vestibular head-orientation information into Earth-reference spatial orientation and self-motion information (Yakusheva et al., 2007). Although the L7PKCI mice had significantly fewer place cells compared with wild-type littermates, place fields were largely unaffected during normal conditions when both idiothetic and landmark information were available . "
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    ABSTRACT: Navigation is a complex cognitive process that is vital for survival. The rodent hippocampus has long been implicated in spatial memory and navigation. Following the discovery of place cells, found in the hippocampus, a variety of other spatially tuned neural correlates of navigation have been found in a widely distributed network that is both anatomically and functionally interconnected with the hippocampus. Angular head velocity, head direction, and grid cells are among some of the additional spatial neural correlates. The importance of these different cells and how they function interdependently to subserve navigation is reviewed below. © 2015 Elsevier B.V. All rights reserved.
    Progress in brain research 06/2015; 219:83-102. DOI:10.1016/bs.pbr.2015.03.004 · 2.83 Impact Factor
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    • "In our mutant mice, Cre/loxP recombination was observed in the cerebellum (Figure 2A), and slight motor abnormalities were found in homozygous mice (see Results), suggesting the possibility that mutated GluN2A in the cerebellum may contribute to the mutant phenotype even in heterozygotes. The cerebellum is known to process self-motion signals [45,46], and a recent report showed that a transgenic mouse line with impaired protein kinase C-dependent plasticity at parallel fiber–Purkinje cell synapses has impaired hippocampal place field activity under specific circumstances, i.e., when animals rely on self-motion cues, or when there is conflict between visual cues and self-motion cues [47]. This report indicated a role for the cerebellum in processing self-motion signals for shaping hippocampal place field activity. "
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    ABSTRACT: Background Voltage-dependent block of the NMDA receptor by Mg2+ is thought to be central to the unique involvement of this receptor in higher brain functions. However, the in vivo role of the Mg2+ block in the mammalian brain has not yet been investigated, because brain-wide loss of the Mg2+ block causes perinatal lethality. In this study, we used a brain-region specific knock-in mouse expressing an NMDA receptor that is defective for the Mg2+ block in order to test its role in neural information processing. Results We devised a method to induce a single amino acid substitution (N595Q) in the GluN2A subunit of the NMDA receptor, specifically in the hippocampal dentate gyrus in mice. This mutation reduced the Mg2+ block at the medial perforant path–granule cell synapse and facilitated synaptic potentiation induced by high-frequency stimulation. The mutants had more stable hippocampal place fields in the CA1 than the controls did, and place representation showed lower sensitivity to visual differences. In addition, behavioral tests revealed that the mutants had a spatial working memory deficit. Conclusions These results suggest that the Mg2+ block in the dentate gyrus regulates hippocampal spatial information processing by attenuating activity-dependent synaptic potentiation in the dentate gyrus.
    Molecular Brain 06/2014; 7(1):44. DOI:10.1186/1756-6606-7-44 · 4.90 Impact Factor
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