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Research ArticleNew Research, Neuronal Excitability

Climbing Fiber Regulation of Spontaneous Purkinje Cell Activity and Cerebellum-Dependent Blink Responses

Riccardo Zucca, Anders Rasmussen and Fredrik Bengtsson
eNeuro 5 January 2016, 3 (1) ENEURO.0067-15.2015; DOI: https://doi.org/10.1523/ENEURO.0067-15.2015
Riccardo Zucca
1Synthetic Perceptive Emotive and Cognitive Systems Laboratory, Center for Autonomous Systems and Neuro-robotics, Information and Communication Technologies Department, Universitat Pompeu Fabra, 08002 Barcelona, Spain
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Anders Rasmussen
2Department of Neuroscience, Erasmus Medical Center, 3000 DR, Rotterdam, The Netherlands
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Fredrik Bengtsson
3Department of Experimental Medical Science, Section for Neurophysiology, Lund University, SE-221 84 Lund, Sweden
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    Figure 1.

    Experimental setup, cerebellar circuit diagram, and single unit records. A, Schematic illustration of the experimental setup with recording and stimulation sites. mf, Mossy fiber; cf, climbing fiber; pf, parallel fiber; PC, Purkinje cell; GrC, granule cell; CN, cerebellar nuclei; IO, inferior olive; SC, superior colliculus. B, Complex spikes evoked by climbing fiber stimulation. Thin black traces represent ten superimposed complex spikes. Thick trace is the average waveform. The asterisk indicates the onset of the complex spike and the black arrow indicates the time of the stimulation. C, Extracellular recording of a representative Purkinje cell. Bottom trace shows an unfiltered recording and the inset shows, in greater detail, the complex spike evoked by climbing fiber stimulation. D, Archetypal interspike interval distribution before the start of the climbing fiber stimulation.

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    Figure 2.

    Stimulating climbing fibers suppresses Purkinje cell activity in a frequency dependent manner. A, Time course of the simple spike suppression in a Purkinje cell during a complete experimental session. Climbing fibers were stimulated with electrical pulses (duration, 0.1 ms; intensity, 240 μA), for 5 min at incremental frequencies, with 60 s breaks in between each switch in frequency. The firing rate was estimated through convoluting the spike train with a Gaussian kernel (sigma, 2 s). B, Change in Purkinje cell activity as a function of the climbing fiber stimulation frequency in each of the five cells, as well as the average change (right). C, Scatterplot illustrating the relation between the climbing fiber stimulation frequency on the x-axis and changes in Purkinje cell activity on the y-axis. The data fits an exponential curve (black line) described by a coefficient of 0.397. The best fit was obtained through the Matlab Curve fitting toolbox (MathWorks). D, Average raster plot of simple spike firing rate changes over time. The color of the shadings indicates simple spike activity changes relative to the pre-stimulation baseline (baseline = 0%). Lighter areas indicate inhibition of simple spike firing (i.e., 100% equals a complete suppression) and darker areas indicate increased activity. E, Time course of the simple spike activity changes over the entire stimulation session averaged for the five experiments. Each data point corresponds to the firing rate change over a 100 ms window. Light gray shadings represent a 95% confidence interval.

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    Figure 3.

    Interspike interval distributions for each climbing fiber stimulation frequency (bin size, 2 ms).

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    Figure 4.

    A, Average of 10 consecutive field potentials recorded on the cerebellar cortex following direct stimulation of climbing fibers. Asterisk indicates the climbing fiber response. B, EMG from the orbicularis oculi muscle recording on a single CS-alone trial in a trained animal. The top trace shows a rectified and smoothed trace (smoothing window 10 ms). The bottom trace shows the raw signal. C, Rectified and smoothed EMG on paired trials without climbing fiber stimulation (top left), CS-alone trials with climbing fiber stimulation at 4 Hz (top right and bottom left), and on CS-alone trials without climbing fiber stimulation (bottom right). D, Effect of sustained climbing fiber stimulation at 1–4.5 Hz on the rate of conditioned eyeblink responses (ECR). Each bar plot shows the percentage of ECRs (+ SEM), in blocks of 10 trials, for each stimulation frequency.

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    Figure 5.

    3D surface plots illustrating orbicularis oculi EMG in one animal in the last three test blocks for each stimulation frequency. Data were rectified and binned over a 50 ms window and normalized to the highest value over the seven recording sessions.

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    Table 1:

    Statistical analysis

    Data structureType of testPower
    a.NormalRepeated-measures ANOVA0.0012
    4 Hz stimulationPost hoc (Bonferroni corrected)0.0067
    5 Hz stimulationPost hoc (Bonferroni corrected)0.00002
    0.5 Hz stimulation (final session)Post hoc (Bonferroni corrected)0.812
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Climbing Fiber Regulation of Spontaneous Purkinje Cell Activity and Cerebellum-Dependent Blink Responses
Riccardo Zucca, Anders Rasmussen, Fredrik Bengtsson
eNeuro 5 January 2016, 3 (1) ENEURO.0067-15.2015; DOI: 10.1523/ENEURO.0067-15.2015

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Climbing Fiber Regulation of Spontaneous Purkinje Cell Activity and Cerebellum-Dependent Blink Responses
Riccardo Zucca, Anders Rasmussen, Fredrik Bengtsson
eNeuro 5 January 2016, 3 (1) ENEURO.0067-15.2015; DOI: 10.1523/ENEURO.0067-15.2015
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Keywords

  • climbing fibers
  • eyeblink conditioning
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  • Simple spikes
  • Spontaneous background firing

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