Electrophysiological studies on the postnatal development of intracerebellar nuclei neurons in rat cerebellar slices maintained in vitro. II. Membrane conductances

Gardette, Robert; Debono, Marc; Dupont, Jean‐Luc; Crépel, F.

doi:10.1016/0165-3806(85)90091-4

Cited by 50 publications

(27 citation statements)

References 43 publications

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“…Furthermore, the RD evoked by a hyperpolarizing pulse was of shorter duration and smaller amplitude and hence was associated with the generation of far fewer spikes. These findings confirm and extend previous observations by Gardette et al (1985b). Using horseradish peroxidase labeling, Bourrat and Sotelo (1986) determined that the main stages of dendritic differentiation in the rat DCN occur between E16 and E19.…”

Section: Discussionsupporting

confidence: 81%

“…DCN neurons are very active at rest and either spike regularly or burst spontaneously (Aizenman and Linden 1999;Czubayko et al 2001;Gardette et al 1985b;Jahnsen 1986a,b;Llinas and Muhlethaler 1988;Raman et al 2000). One important characteristic is that DCN neurons will exhibit a pronounced rebound depolarization (RD) that typically triggers a series of action potentials immediately after the offset of a hyperpolarizing pulse or a train of inhibitory postsynaptic potentials (IPSPs).…”

Section: Introductionmentioning

confidence: 99%

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Morphological Correlates of Intrinsic Electrical Excitability in Neurons of the Deep Cerebellar Nuclei

Aizenman

Huang

Linden

2003

Journal of Neurophysiology

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phological correlates of intrinsic electrical excitability in neurons of the deep cerebellar nuclei. J Neurophysiol 89: 1738 -1747, 2003; 10.1152/jn.01043.2002. To what degree does neuronal morphology determine or correlate with intrinsic electrical properties within a particular class of neuron? This question has been examined using microelectrode recordings and subsequent neurobiotin filling and reconstruction of neurons in the deep cerebellar nuclei (DCN) of brain slices from young rats (P13-16). The neurons reconstructed from these recordings were mostly large and multipolar (17/21 cells) and were likely to represent glutamatergic projection neurons. Within this class, there was considerable variation in intrinsic electrical properties and cellular morphology. Remarkably, in a correlation matrix of 18 electrophysiological and 6 morphological measures, only one morphological characteristic was predictive of intrinsic excitability: neurons with more spines had a significantly slower basal firing rate. To address the possibility that neurons with fewer spines represented a slowly maturing subgroup, recordings and reconstructions were also made from neurons at a younger age (P6 -9). While P6 -9 neurons were morphologically indistinguishable from P13 to 16 neurons, they were considerably less excitable: P6 -9 neurons had a lower spontaneous spiking rate, larger fast AHPs, higher resting membrane potentials, and smaller rebound depolarizations. Thus while the large projection neurons of the DCN are morphologically mature by P6 -9, they continue to mature electrophysiologically through P13-16 in a way that renders them more responsive to the burst-and-pause pattern that characterizes Purkinje cell inhibitory synaptic drive. I N T R O D U C T I O NThe deep cerebellar nuclei (DCN) are at the center of the cerebellar circuitry and form its primary output structure. In the DCN, a variety of excitatory and inhibitory projections, representing several streams of sensory-motor information, converge. Purkinje cells, which constitute the sole output of the cerebellar cortex, send GABAergic inhibitory projections to the DCN. Additionally, the DCN receive glutamatergic excitatory inputs from various precerebellar nuclei and the inferior olive via mossy fibers and climbing fibers, respectively. The firing patterns of the DCN neurons will therefore reflect the sum of all the neural computations that are performed in the cerebellar system that are then translated into a variety of motor outputs. There is increasing evidence that the DCN and an analogous structure, the vestibular nuclei, play an important role in several types of motor learning, including associative eyelid conditioning and adaptation of the vestibulo-ocular re-

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Section: Discussionsupporting

confidence: 81%

Section: Introductionmentioning

confidence: 99%

Morphological Correlates of Intrinsic Electrical Excitability in Neurons of the Deep Cerebellar Nuclei

Aizenman

Huang

Linden

2003

Journal of Neurophysiology

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“…We therefore propose that the initial maturation of excitability, between stage 42/43 and stages 44 -46, represents a maturational program that follows along similar lines as has been described for several cell types in which intrinsic excitability increases developmentally (Gardette et al, 1985;MacDermott and Westbrook, 1986;Ramoa and McCormick, 1994;Spitzer and Ribera, 1998). In contrast, we propose that the decrease in excitability occurring by stage 49 may be attributable to an activitydriven downregulation of voltage-gated Na ϩ currents.…”

Section: Developmental Regulation Of Intrinsic Excitabilitymentioning

confidence: 51%

Homeostatic Regulation of Intrinsic Excitability and Synaptic Transmission in a Developing Visual Circuit

Pratt¹,

Aizenman²

2007

J. Neurosci.

143

163

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One of the major challenges faced by the developing visual system is how to stably process visual information, yet at the same time remain flexible enough to accommodate growth and plasticity induced by visual experience. We find that in the Xenopus retinotectal circuit, during a period in development when the retinotectal map undergoes activity-dependent refinement and visual inputs strengthen, tectal neurons adapt their intrinsic excitability such that a stable relationship between the total level of synaptic input and tectal neuron spike output is conserved. This homeostatic balance between synaptic and intrinsic properties is maintained, in part, via regulation of voltagegated Na ϩ currents, resulting in a stable neuronal input-output function. We experimentally manipulated intrinsic excitability or synapse strengthening in developing tectal neurons in vivo by electroporation of a leak K ϩ channel gene or a peptide that interferes with normal AMPA receptor trafficking. Both manipulations resulted in a compensatory increase in voltage-gated Na ϩ currents. This suggests that intrinsic neuronal properties are actively regulated as a function of the total level of neuronal activity experienced during development. We conclude that the coordinated changes between synaptic and intrinsic properties allow developing optic tectal neurons to remain within a stable dynamic range, even as the pattern and strength of visual inputs changes over development, suggesting that homeostatic regulation of intrinsic properties plays a central role in the functional development of neural circuits.

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“…3 A and B). A similar phenomenon has previously been reported at the synapse formed between Purkinje cells and deep cerebellar nuclei (26)(27)(28). However, if the Purkinje cell was already in an up state when the GABA A conductance occurred, the resulting IPSP caused a deep hyperpolarization of the cell membrane beyond the reversal potential for GABA.…”

Section: Discussionmentioning

confidence: 79%

Interneurons of the cerebellar cortex toggle Purkinje cells between up and down states

Oldfield

Marty

Stell

2010

Proc. Natl. Acad. Sci. U.S.A.

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We demonstrate that single interneurons can toggle the output neurons of the cerebellar cortex (the Purkinje cells) between their two states. The firing of Purkinje cells has previously been shown to alternate between an "up" state in which the cell fires spontaneous action potentials and a silent "down" state. We show here that small hyperpolarizing currents in Purkinje cells can bidirectionally toggle Purkinje cells between down and up states and that blockade of the hyperpolarization-activated cation channels (H channels) with the specific antagonist ZD7288 (10 μM) blocks the transitions from down to up states. Likewise, hyperpolarizing inhibitory postsnyaptic potentials (IPSPs) produced by small bursts of action potentials (10 action potentials at 50 Hz) in molecularlayer interneurons induce these bidirectional transitions in Purkinje cells. Furthermore, single interneurons in paired interneuron → Purkinje cell recordings, produce bidirectional switches between the two states of Purkinje cells. The ability of molecular-layer interneurons to toggle Purkinje cells occurs when Purkinje cells are recorded under whole-cell patch-clamp conditions as well as when action potentials are recorded in an extracellular loose cell-attached configuration. The mode switch demonstrated here indicates that a single presynaptic interneuron can have opposite effects on the output of a given Purkinje cell, which introduces a unique type of synaptic interaction that may play an important role in cerebellar signaling.A s the sole output of the cerebellar cortex, Purkinje cells are ultimately responsible for relaying the computation performed by the entire network. Even though membrane properties and synaptic currents have been extensively studied in the cerebellar circuit, it still remains unclear how Purkinje cells process information coming from the rest of the cerebellar cortex before passing it on to the deep cerebellar nuclei. Purkinje cells are known to intrinsically generate action potentials at high rates and also to have an intrinsic membrane bistability (1-4). The cell switches between hyperpolarized potentials during which it is silent and depolarized potentials during which it fires action potentials (1, 2, 5-11). The frequency of changes between the two states in awake versus anesthetized animals in vivo has been disputed, but it is agreed that the bistability exists in a fraction of Purkinje cells in both anesthetized and unanesthetized animals (5, 6). This unique characteristic of the output of Purkinje cells potentially plays a significant role in passing the computation of the cerebellar cortex onto the cerebellar nuclei. Therefore to understand how Purkinje cells process this information it is essential to understand how the cells within the cerebellar cortex influence this bistable output of Purkinje cells.The climbing fibers, which provide glutamatergic inputs to Purkinje cells from outside the cerebellar cortex, have been shown to produce complex spikes in Purkinje cells (1). In experiments performed in vivo a...

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Electrophysiological studies on the postnatal development of intracerebellar nuclei neurons in rat cerebellar slices maintained in vitro. II. Membrane conductances

Cited by 50 publications

References 43 publications

Morphological Correlates of Intrinsic Electrical Excitability in Neurons of the Deep Cerebellar Nuclei

Morphological Correlates of Intrinsic Electrical Excitability in Neurons of the Deep Cerebellar Nuclei

Homeostatic Regulation of Intrinsic Excitability and Synaptic Transmission in a Developing Visual Circuit

Interneurons of the cerebellar cortex toggle Purkinje cells between up and down states

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