scholarly journals Potentiation of cerebellar Purkinje cells facilitates whisker reflex adaptation through increased simple spike activity

2018 ◽  
Author(s):  
Vincenzo Romano ◽  
Licia De Propris ◽  
Laurens W.J. Bosman ◽  
Pascal Warnaar ◽  
Michiel M. ten Brinke ◽  
...  
Keyword(s):  
Purkinje Cell ◽  
Purkinje Cells ◽  
Spike Activity ◽  
Cell Activity ◽  
Response Probability ◽  
Long Term Potentiation ◽  
Parallel Fiber ◽  
Spike Response ◽  
Simple Spike ◽  
Cerebellar Plasticity

SummaryCerebellar plasticity underlies motor learning. However, how the cerebellum operates to enable learned changes in motor output is largely unknown. We developed a sensory-driven adaptation protocol for reflexive whisker protraction and recorded Purkinje cell activity from crus 1 and 2 of awake mice. Before training, simple spikes of individual Purkinje cells correlated during reflexive protraction with the whisker position without lead or lag. After training, simple spikes and whisker protractions were both enhanced with the spiking activity now leading the behavioral response. Neuronal and behavior changes did not occur in two cell-specific mouse models with impaired long-term potentiation at parallel fiber to Purkinje cell synapses. Consistent with cerebellar plasticity rules, increased simple spike activity was prominent in cells with low complex spike response probability. Thus, potentiation at parallel fiber to Purkinje cell synapses may contribute to reflex adaptation and enable expression of cerebellar learning through increases in simple spike activity.Impact statementRomano et al. show that expression of cerebellar whisker learning can be mediated by increases in simple spike activity, depending on LTP induction at parallel fiber to Purkinje cell synapses.

scholarly journals Potentiation of cerebellar Purkinje cells facilitates whisker reflex adaptation through increased simple spike activity

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Vincenzo Romano ◽  
Licia De Propris ◽  
Laurens WJ Bosman ◽  
Pascal Warnaar ◽  
Michiel M ten Brinke ◽  
...  
Keyword(s):  
Purkinje Cell ◽  
Purkinje Cells ◽  
Spike Activity ◽  
Cell Activity ◽  
Response Probability ◽  
Long Term Potentiation ◽  
Parallel Fiber ◽  
Spike Response ◽  
Simple Spike ◽  
Cerebellar Plasticity

Cerebellar plasticity underlies motor learning. However, how the cerebellum operates to enable learned changes in motor output is largely unknown. We developed a sensory-driven adaptation protocol for reflexive whisker protraction and recorded Purkinje cell activity from crus 1 and 2 of awake mice. Before training, simple spikes of individual Purkinje cells correlated during reflexive protraction with the whisker position without lead or lag. After training, simple spikes and whisker protractions were both enhanced with the spiking activity now leading behavioral responses. Neuronal and behavioral changes did not occur in two cell-specific mouse models with impaired long-term potentiation at their parallel fiber to Purkinje cell synapses. Consistent with cerebellar plasticity rules, increased simple spike activity was prominent in cells with low complex spike response probability. Thus, potentiation at parallel fiber to Purkinje cell synapses may contribute to reflex adaptation and enable expression of cerebellar learning through increases in simple spike activity.

scholarly journals Purkinje Cell Representations of Behavior: Diary of a Busy Neuron

2018 ◽  
Vol 25 (3) ◽  
pp. 241-257 ◽  
Author(s):  
Laurentiu S. Popa ◽  
Martha L. Streng ◽  
Timothy J. Ebner
Keyword(s):  
Purkinje Cell ◽  
Purkinje Cells ◽  
Motor Behavior ◽  
Cell Activity ◽  
Computational Framework ◽  
Simple Spike ◽  
Cerebellar Function ◽  
Performance Error ◽  
And Performance ◽  
High Degree

Fundamental for understanding cerebellar function is determining the representations in Purkinje cell activity, the sole output of the cerebellar cortex. Up to the present, the most accurate descriptions of the information encoded by Purkinje cells were obtained in the context of motor behavior and reveal a high degree of heterogeneity of kinematic and performance error signals encoded. The most productive framework for organizing Purkinje cell firing representations is provided by the forward internal model hypothesis. Direct tests of this hypothesis show that individual Purkinje cells encode two different forward models simultaneously, one for effector kinematics and one for task performance. Newer results demonstrate that the timing of simple spike encoding of motor parameters spans an extend interval of up to ±2 seconds. Furthermore, complex spike discharge is not limited to signaling errors, can be predictive, and dynamically controls the information in the simple spike firing to meet the demands of upcoming behavior. These rich, diverse, and changing representations highlight the integrative aspects of cerebellar function and offer the opportunity to generalize the cerebellar computational framework over both motor and non-motor domains.

scholarly journals Anoctamin 2-chloride channels reduce simple spike activity and mediate inhibition at elevated calcium concentration in cerebellar Purkinje cells

PLoS ONE ◽  
2021 ◽  
Vol 16 (3) ◽  
pp. e0247801
Author(s):  
Friederike Auer ◽  
Eliana Franco Taveras ◽  
Uli Klein ◽  
Céline Kesenheimer ◽  
Dana Fleischhauer ◽  
...  
Keyword(s):  
Purkinje Cells ◽  
Spike Activity ◽  
Chloride Channels ◽  
Cell Activity ◽  
High Threshold ◽  
Chloride Currents ◽  
Simple Spike ◽  
Cerebellar Purkinje Cells ◽  
Inferior Olivary

Modulation of neuronal excitability is a prominent way of shaping the activity of neuronal networks. Recent studies highlight the role of calcium-activated chloride currents in this context, as they can both increase or decrease excitability. The calcium-activated chloride channel Anoctamin 2 (ANO2 alias TMEM16B) has been described in several regions of the mouse brain, including the olivo-cerebellar system. In inferior olivary neurons, ANO2 was proposed to increase excitability by facilitating the generation of high-threshold calcium spikes. An expression of ANO2 in cerebellar Purkinje cells was suggested, but its role in these neurons remains unclear. In the present study, we confirmed the expression of Ano2 mRNA in Purkinje cells and performed electrophysiological recordings to examine the influence of ANO2-chloride channels on the excitability of Purkinje cells by comparing wildtype mice to mice lacking ANO2. Recordings were performed in acute cerebellar slices of adult mice, which provided the possibility to study the role of ANO2 within the cerebellar cortex. Purkinje cells were uncoupled from climbing fiber input to assess specifically the effect of ANO2 channels on Purkinje cell activity. We identified an attenuating effect of ANO2-mediated chloride currents on the instantaneous simple spike activity both during strong current injections and during current injections close to the simple spike threshold. Moreover, we report a reduction of inhibitory currents from GABAergic interneurons upon depolarization, lasting for several seconds. Together with the role of ANO2-chloride channels in inferior olivary neurons, our data extend the evidence for a role of chloride-dependent modulation in the olivo-cerebellar system that might be important for proper cerebellum-dependent motor coordination and learning.

scholarly journals Differential Purkinje cell simple spike activity and pausing behavior related to cerebellar modules

2015 ◽  
Vol 113 (7) ◽  
pp. 2524-2536 ◽  
Author(s):  
Haibo Zhou ◽  
Kai Voges ◽  
Zhanmin Lin ◽  
Chiheng Ju ◽  
Martijn Schonewille
Keyword(s):  
Purkinje Cell ◽  
Purkinje Cells ◽  
Cerebellar Cortex ◽  
Spike Activity ◽  
Vestibular Nuclei ◽  
Simple Spike ◽  
Transverse Zone ◽  
Cerebellar Modules ◽  
Lower Temperature ◽  
Cerebellar Purkinje Cells

The massive computational capacity of the cerebellar cortex is conveyed by Purkinje cells onto cerebellar and vestibular nuclei neurons through their GABAergic, inhibitory output. This implies that pauses in Purkinje cell simple spike activity are potentially instrumental in cerebellar information processing, but their occurrence and extent are still heavily debated. The cerebellar cortex, although often treated as such, is not homogeneous. Cerebellar modules with distinct anatomical connectivity and gene expression have been described, and Purkinje cells in these modules also differ in firing rate of simple and complex spikes. In this study we systematically correlate, in awake mice, the pausing in simple spike activity of Purkinje cells recorded throughout the entire cerebellum, with their location in terms of lobule, transverse zone, and zebrin-identified cerebellar module. A subset of Purkinje cells displayed long (>500-ms) pauses, but we found that their occurrence correlated with tissue damage and lower temperature. In contrast to long pauses, short pauses (<500 ms) and the shape of the interspike interval (ISI) distributions can differ between Purkinje cells of different lobules and cerebellar modules. In fact, the ISI distributions can differ both between and within populations of Purkinje cells with the same zebrin identity, and these differences are at least in part caused by differential synaptic inputs. Our results suggest that long pauses are rare but that there are differences related to shorter intersimple spike intervals between and within specific subsets of Purkinje cells, indicating a potential further segregation in the activity of cerebellar Purkinje cells.

scholarly journals Calcium imaging reveals coordinated simple spike pauses in populations of Cerebellar Purkinje cells

2016 ◽  
Author(s):  
Jorge E. Ramirez ◽  
Brandon M. Stell
Keyword(s):  
Purkinje Cell ◽  
Purkinje Cells ◽  
Calcium Imaging ◽  
Spatial Organization ◽  
Cell Activity ◽  
Cerebellar Nuclei ◽  
Deep Cerebellar Nuclei ◽  
Firing Rates ◽  
Simple Spike ◽  
Cerebellar Purkinje Cells

The brain’s control of movement is thought to involve coordinated activity between cerebellar Purkinje cells. The results reported here demonstrate that somatic Ca2+ imaging is a faithful reporter of Na+-dependent “simple spike” pauses and enables us to optically record changes in firing rates in populations of Purkinje cells. This simultaneous calcium imaging of populations of Purkinje cells reveals a striking spatial organization of pauses in Purkinje cell activity between neighboring cells. The source of this organization is shown to be the presynaptic GABAergic network and blocking GABAARs abolishes the synchrony. These data suggest that presynaptic interneurons synchronize (in)activity between neighboring Purkinje cells and thereby maximize their effect on downstream targets in the deep cerebellar nuclei.

scholarly journals In vivo analysis of Purkinje cell firing properties during postnatal mouse development

2015 ◽  
Vol 113 (2) ◽  
pp. 578-591 ◽  
Author(s):  
Marife Arancillo ◽  
Joshua J. White ◽  
Tao Lin ◽  
Trace L. Stay ◽  
Roy V. Sillitoe
Keyword(s):  
Purkinje Cell ◽  
Purkinje Cells ◽  
Motor Behavior ◽  
Developmental Trajectories ◽  
Cell Activity ◽  
Mouse Development ◽  
Complex Spike ◽  
Simple Spike ◽  
Spike Firing

Purkinje cell activity is essential for controlling motor behavior. During motor behavior Purkinje cells fire two types of action potentials: simple spikes that are generated intrinsically and complex spikes that are induced by climbing fiber inputs. Although the functions of these spikes are becoming clear, how they are established is still poorly understood. Here, we used in vivo electrophysiology approaches conducted in anesthetized and awake mice to record Purkinje cell activity starting from the second postnatal week of development through to adulthood. We found that the rate of complex spike firing increases sharply at 3 wk of age whereas the rate of simple spike firing gradually increases until 4 wk of age. We also found that compared with adult, the pattern of simple spike firing during development is more irregular as the cells tend to fire in bursts that are interrupted by long pauses. The regularity in simple spike firing only reached maturity at 4 wk of age. In contrast, the adult complex spike pattern was already evident by the second week of life, remaining consistent across all ages. Analyses of Purkinje cells in alert behaving mice suggested that the adult patterns are attained more than a week after the completion of key morphogenetic processes such as migration, lamination, and foliation. Purkinje cell activity is therefore dynamically sculpted throughout postnatal development, traversing several critical events that are required for circuit formation. Overall, we show that simple spike and complex spike firing develop with unique developmental trajectories.

Increase in Purkinje cell gain associated with naturally activated climbing fiber input

1983 ◽  
Vol 50 (1) ◽  
pp. 205-219 ◽  
Author(s):  
T. J. Ebner ◽  
Q. X. Yu ◽  
J. R. Bloedel
Keyword(s):  
Purkinje Cell ◽  
Purkinje Cells ◽  
Mossy Fiber ◽  
Climbing Fiber ◽  
Peripheral Stimulus ◽  
Short Term ◽  
Spike Response ◽  
Complex Spike ◽  
Simple Spike ◽  
Complex Spikes

These experiments were designed to test the hypothesis that climbing fiber inputs evoked by a peripheral stimulus increase the responsiveness of Purkinje cells to mossy fiber inputs. This hypothesis was based on a previous series of observations demonstrating that spontaneous climbing fiber inputs are associated with an accentuation of the Purkinje cell responses to subsequent mossy fiber inputs (10, 12). Furthermore, short-term nonpersistent interactions between climbing and mossy fiber inputs have been an important aspect of many theories of cerebellar function (5, 7, 8, 12, 36). Extracellular unitary recordings were made from Purkinje cells in lobule V of decerebrate, unanesthetized cats. To activate mossy and climbing fiber inputs, the forepaw was passively flexed by a Ling vibrator system. A data analysis was developed to sort the simple spike trials into two groups, based on the presence or absence of complex spikes activated by the stimulus. In addition, during those trials in which complex spikes were activated, the simple spike train was aligned on the occurrence of the complex spike. For each simple spike response to the forepaw input, the average firing rate during the response was compared to background both in those trials in which complex spikes were activated and in those in which they were not. The ratio of the response amplitudes in the histograms constructed from these two groups of trials permitted a quantification of the change in responsiveness when climbing fiber inputs were activated. The results show that both excitatory and inhibitory simple spike responses are accentuated when associated with the activation of a complex spike. Using an arbitrary level of a gain change ratio of 120% as indicating a significant modification, 64% of the response components analyzed increased their amplitude when climbing fiber input was present. Simple spike response components occurring prior to complex spike activation were usually not accentuated, although in a few cells the amplitude of this component of the response increased. In addition, in a small number of cells the occurrence of complex spikes was associated with a new simple spike component. For excitatory responses, the magnitude of the gain change ratio was shown to be inversely related to the amplitude of the simple spike response evoked by the mossy fiber inputs. The data obtained is consistent with the hypothesis that the climbing fiber input is associated with an increase in the responsiveness of Purkinje cells to mossy fiber inputs. The increased responsiveness occurs whether the simple spike modulation evoked by the peripheral stimulus is excitatory or inhibitory. The change in responsiveness is short term and nonpersistent. It is argued that the activation of climbing fiber inputs to the cerebellar cortex is associated with an increase in the gain of Purkinje cells to mossy fiber inputs activated by natural peripheral stimuli.

scholarly journals Current source density correlates of cerebellar Golgi and Purkinje cell responses to tactile input

2011 ◽  
Vol 105 (3) ◽  
pp. 1327-1341 ◽  
Author(s):  
Koen Tahon ◽  
Mike Wijnants ◽  
Erik De Schutter ◽  
Reinoud Maex
Keyword(s):  
Purkinje Cell ◽  
Purkinje Cells ◽  
Spike Activity ◽  
Granular Layer ◽  
Current Source ◽  
Current Source Density ◽  
Golgi Cell ◽  
Golgi Cells ◽  
Source Density ◽  
Simple Spike

The overall circuitry of the cerebellar cortex has been known for over a century, but the function of many synaptic connections remains poorly characterized in vivo. We used a one-dimensional multielectrode probe to estimate the current source density (CSD) of Crus IIa in response to perioral tactile stimuli in anesthetized rats and to correlate current sinks and sources to changes in the spike rate of corecorded Golgi and Purkinje cells. The punctate stimuli evoked two distinct early waves of excitation (at <10 and ∼20 ms) associated with current sinks in the granular layer. The second wave was putatively of corticopontine origin, and its associated sink was located higher in the granular layer than the first trigeminal sink. The distinctive patterns of granular-layer sinks correlated with the spike responses of corecorded Golgi cells. In general, Golgi cell spike responses could be linearly reconstructed from the CSD profile. A dip in simple-spike activity of coregistered Purkinje cells correlated with a current source deep in the molecular layer, probably generated by basket cell synapses, interspersed between sparse early sinks presumably generated by synapses from granule cells. The late (>30 ms) enhancement of simple-spike activity in Purkinje cells was characterized by the absence of simultaneous sinks in the granular layer and by the suppression of corecorded Golgi cell activity, pointing at inhibition of Golgi cells by Purkinje axon collaterals as a likely mechanism of late Purkinje cell excitation.

scholarly journals Functional convergence of autonomic and sensorimotor processing in the lateral cerebellum

2019 ◽  
Author(s):  
Vincenzo Romano ◽  
Aoibhinn L. Reddington ◽  
Silvia Cazzanelli ◽  
Mario Negrello ◽  
Laurens W.J. Bosman ◽  
...  
Keyword(s):  
Purkinje Cell ◽  
Ampa Receptors ◽  
Spike Activity ◽  
Cell Activity ◽  
Respiratory Control ◽  
Dependent Manner ◽  
Sensorimotor Processing ◽  
Simple Spike ◽  
Whisker Stimulation ◽  
The Impact

The cerebellum is involved in control of voluntary and autonomic rhythmic behaviors, yet it is largely unclear to what extent it coordinates these in a concerted action. Here, we studied Purkinje cell activity during unperturbed and perturbed respiration in cerebellar lobules simplex, crus 1 and 2. During unperturbed (eupneic) respiration complex spike and simple spike activity encoded respiratory activity, the timing of which corresponded with ongoing sensorimotor feedback. Instead, upon whisker stimulation mice concomitantly accelerated their simple spike activity and inspiration in a phase-dependent manner. Moreover, the accelerating impact of whisker stimulation on respiration could be mimicked by optogenetic stimulation of Purkinje cells and prevented by cell-specific genetic modification of their AMPA receptors that hampered increases in simple spike firing. Thus, the impact of Purkinje cell activity on respiratory control is context- and phase-dependent, suggesting a coordinating role for the cerebellar hemispheres in aligning autonomic and sensorimotor behaviors.

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