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      Purkinje neuron synchrony elicits time-locked spiking in the cerebellar nuclei

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          Abstract

          An unusual feature of the cerebellar cortex is that its output neurons, Purkinje cells, are GABAergic. Their high intrinsic firing rates 1 (50 Hz) and extensive convergence 2, 3 predict that that target neurons in the cerebellar nuclei would be largely inhibited unless Purkinje cells pause their spiking, yet Purkinje and nuclear neuron firing rates do not always vary inversely 4 . A potential clue to how these synapses transmit information is that populations of Purkinje neurons synchronize their spikes during cerebellar behaviors 511 . If nuclear neurons respond to Purkinje synchrony, they may encode signals from subsets of inhibitory inputs 7, 1214 . Here we show in weanling and adult mice that nuclear neurons transmit the timing of synchronous Purkinje afferent spikes, owing to modest Purkinje-to-nuclear convergence ratios (~40:1), fast IPSC kinetics (τ decay=2.5 ms), and high intrinsic firing rates (~90 Hz). In vitro, dynamically clamped asynchronous IPSPs mimicking Purkinje afferents suppress nuclear cell spiking, whereas synchronous IPSPs entrain nuclear cell spiking. With partial synchrony, nuclear neurons time-lock their spikes to the synchronous subpopulation of inputs, even when only 2 of 40 afferents synchronize. In vivo, nuclear neurons reliably phase-lock to regular trains of molecular layer stimulation. Thus, cerebellar nuclear neurons can preferentially relay the spike timing of synchronized Purkinje cells to downstream premotor areas.

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          Most cited references30

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          The neural basis of temporal processing.

          A complete understanding of sensory and motor processing requires characterization of how the nervous system processes time in the range of tens to hundreds of milliseconds (ms). Temporal processing on this scale is required for simple sensory problems, such as interval, duration, and motion discrimination, as well as complex forms of sensory processing, such as speech recognition. Timing is also required for a wide range of motor tasks from eyelid conditioning to playing the piano. Here we review the behavioral, electrophysiological, and theoretical literature on the neural basis of temporal processing. These data suggest that temporal processing is likely to be distributed among different structures, rather than relying on a centralized timing area, as has been suggested in internal clock models. We also discuss whether temporal processing relies on specialized neural mechanisms, which perform temporal computations independent of spatial ones. We suggest that, given the intricate link between temporal and spatial information in most sensory and motor tasks, timing and spatial processing are intrinsic properties of neural function, and specialized timing mechanisms such as delay lines, oscillators, or a spectrum of different time constants are not required. Rather temporal processing may rely on state-dependent changes in network dynamics.
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            Direct and indirect activation of cortical neurons by electrical microstimulation.

            Electrical microstimulation has been used to elucidate cortical function. This review discusses neuronal excitability and effective current spread estimated by using three different methods: 1) single-cell recording, 2) behavioral methods, and 3) functional magnetic resonance imaging (fMRI). The excitability properties of the stimulated elements in neocortex obtained using these methods were found to be comparable. These properties suggested that microstimulation activates the most excitable elements in cortex, that is, by and large the fibers of the pyramidal cells. Effective current spread within neocortex was found to be greater when measured with fMRI compared with measures based on single-cell recording or behavioral methods. The spread of activity based on behavioral methods is in close agreement with the spread based on the direct activation of neurons (as opposed to those activated synaptically). We argue that the greater activation with imaging is attributed to transynaptic spread, which includes subthreshold activation of sites connected to the site of stimulation. The definition of effective current spread therefore depends on the neural event being measured.
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              High-frequency organization and synchrony of activity in the purkinje cell layer of the cerebellum.

              The cerebellum controls complex, coordinated, and rapid movements, a function requiring precise timing abilities. However, the network mechanisms that underlie the temporal organization of activity in the cerebellum are largely unexplored, because in vivo recordings have usually targeted single units. Here, we use tetrode and multisite recordings to demonstrate that Purkinje cell activity is synchronized by a high-frequency (approximately 200 Hz) population oscillation. We combine pharmacological experiments and modeling to show how the recurrent inhibitory connections between Purkinje cells are sufficient to generate these oscillations. A key feature of these oscillations is a fixed population frequency that is independent of the firing rates of the individual cells. Convergence in the deep cerebellar nuclei of Purkinje cell activity, synchronized by these oscillations, likely organizes temporally the cerebellar output.
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                Author and article information

                Journal
                0410462
                6011
                Nature
                Nature
                Nature
                0028-0836
                1476-4687
                29 November 2011
                25 December 2011
                26 July 2012
                : 481
                : 7382
                : 502-505
                Affiliations
                Department of Neurobiology, Northwestern University. Evanston, IL 60208
                Author notes
                Address for Correspondence: I.M. Raman and A.L. Person, Department of Neurobiology, 2205 Tech Drive, Northwestern University, Evanston IL 60208, Phone: 847-467-7912, 847-467-7905 Fax: 847-491-5211, i-raman@ 123456northwestern.edu , a-person@ 123456northwestern.edu
                Article
                nihpa340423
                10.1038/nature10732
                3268051
                22198670
                76e5f2dc-0005-4552-b884-845cce49f502

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