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: 15.98). 07/2007; 54(6):973-85. DOI: 10.1016/j.neuron.2007.06.003
Source: PubMed

ABSTRACT 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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Available from: Pablo M Blazquez, Jul 16, 2015
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    • "be used to resolve head movements into changes in orientation and motion in the planes of the environment . Interestingly , controlling and referencing the velocity storage response to gravity is also related to the vestibular pathway that connects to the nodulus and uvula ( Solomon and Cohen , 1994 ; Wearne et al . , 1998 ; Cohen et al . , 2002 ; Yakusheva et al . , 2007 ; Laurens et al . , 2013 ) . As discussed above , these parts of the cau - dal cerebellum may provide a similar reference control for the ascending angular velocity signal in the NPH ( Carleton and Carpenter , 1983 ; Horowitz et al . , 2005 ) , and would reference the AHV signal sent to the HD circuit by aligning the head rotation with "
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    ABSTRACT: Head direction (HD) cells have been identified in a number of limbic system structures. These cells encode the animal's perceived directional heading in the horizontal plane and are dependent on an intact vestibular system. Previous studies have reported that the responses of vestibular neuron within the vestibular nuclei are markedly attenuated when an animal makes a volitional head turn compared to passive rotation. This finding presents a conundrum in that if vestibular responses are suppressed during an active head turn how is a vestibular signal propagated forward to drive and update the HD signal? This review identifies and discusses four possible mechanisms that could resolve this problem. These mechanisms are: 1) the ascending vestibular signal is generated by more than just vestibular-only neurons, 2) not all vestibular-only neurons contributing to the HD pathway have firing rates that are attenuated by active head turns, 3) the ascending pathway may be spared from the affects of the attenuation in that the HD system receives information from other vestibular brainstem sites that do not include vestibular-only cells, 4) the ascending signal is affected by the inhibited vestibular signal during an active head turn, but the HD circuit compensates and uses the altered signal to accurately update the current head direction. Future studies will be needed to decipher which of these possibilities is correct.
    Neuroscience 04/2014; 270. DOI:10.1016/j.neuroscience.2014.03.053 · 3.33 Impact Factor
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    • "Additionally, vestibular cerebellar Purkinje cells encode head attitude, that is, orientation in space (Yakusheva et al. 2007), the maintenance of which is critical for a dancer coming out of a pirouette. These data combined with our current findings emphasize the importance of the vestibular cerebellum in the differential processing of vestibular-ocular versus perceptual signals. "
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    ABSTRACT: Sensory input evokes low-order reflexes and higher-order perceptual responses. Vestibular stimulation elicits vestibular-ocular reflex (VOR) and self-motion perception (e.g., vertigo) whose response durations are normally equal. Adaptation to repeated whole-body rotations, for example, ballet training, is known to reduce vestibular responses. We investigated the neuroanatomical correlates of vestibular perceptuo-reflex adaptation in ballet dancers and controls. Dancers' vestibular-reflex and perceptual responses to whole-body yaw-plane step rotations were: (1) Briefer and (2) uncorrelated (controls' reflex and perception were correlated). Voxel-based morphometry showed a selective gray matter (GM) reduction in dancers' vestibular cerebellum correlating with ballet experience. Dancers' vestibular cerebellar GM density reduction was related to shorter perceptual responses (i.e. positively correlated) but longer VOR duration (negatively correlated). Contrastingly, controls' vestibular cerebellar GM density negatively correlated with perception and VOR. Diffusion-tensor imaging showed that cerebral cortex white matter (WM) microstructure correlated with vestibular perception but only in controls. In summary, dancers display vestibular perceptuo-reflex dissociation with the neuronatomical correlate localized to the vestibular cerebellum. Controls' robust vestibular perception correlated with a cortical WM network conspicuously absent in dancers. Since primary vestibular afferents synapse in the vestibular cerebellum, we speculate that a cerebellar gating of perceptual signals to cortical regions mediates the training-related attenuation of vestibular perception and perceptuo-reflex uncoupling.
    Cerebral Cortex 09/2013; 25(2). DOI:10.1093/cercor/bht266 · 8.67 Impact Factor
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    • "Indeed both movements are identical in the head reference frame [displacement vectors (in blue) project onto the x-axis] whereas they are different in the world coordinates (displacement vectors project either onto the x-axis or onto the y-axis). These two movements can be distinguished by taking into account the head position in space, which can be extracted from the combination of semicircular and otolith organs signals (Yakusheva et al., 2007). Column (B) illustrates two movements corresponding to the same head motion in space, but different body motions in space (i.e., on the right the body is stationary). "
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    ABSTRACT: Early investigations of cerebellar function focused on motor learning, in particular on eyeblink conditioning and adaptation of the vestibulo-ocular reflex, and led to the general view that cerebellar long-term depression (LTD) at parallel fiber (PF)-Purkinje cell (PC) synapses is the neural correlate of cerebellar motor learning. Thereafter, while the full complexity of cerebellar plasticities was being unraveled, cerebellar involvement in more cognitive tasks-including spatial navigation-was further investigated. However, cerebellar implication in spatial navigation remains a matter of debate because motor deficits frequently associated with cerebellar damage often prevent the dissociation between its role in spatial cognition from its implication in motor function. Here, we review recent findings from behavioral and electrophysiological analyses of cerebellar mutant mouse models, which show that the cerebellum might participate in the construction of hippocampal spatial representation map (i.e., place cells) and thereby in goal-directed navigation. These recent advances in cerebellar research point toward a model in which computation from the cerebellum could be required for spatial representation and would involve the integration of multi-source self-motion information to: (1) transform the reference frame of vestibular signals and (2) distinguish between self- and externally-generated vestibular signals. We eventually present herein anatomical and functional connectivity data supporting a cerebello-hippocampal interaction. Whilst a direct cerebello-hippocampal projection has been suggested, recent investigations rather favor a multi-synaptic pathway involving posterior parietal and retrosplenial cortices, two regions critically involved in spatial navigation.
    Frontiers in Neural Circuits 03/2013; 7:35. DOI:10.3389/fncir.2013.00035 · 2.95 Impact Factor
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