Dendritic plateau potentials evoked in Purkinje cells by parallel fibre volleys in the cat (original) (raw)
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The Journal of Physiology, 1983
The plateau-like depolarizing potentials evoked in Purkinje cell dendrites by impulses in climbing fibres (Ekerot & Oscarsson, 1981) were conditioned by single parallel fibre volleys and investigated by intra-and extracellular recording from cat cerebellar cortex. The conditioning parallel fibre volleys evoked predominantly inhibitory potentials of long duration in the Purkinje cell dendrites. Massive parallel fibre volleys, which may evoke plateau-like depolarizing potentials (Campbell, Ekerot, Hesslow & Oscarsson, 1983) were avoided. 2. In proximal dendrites parallel fibre volleys preceding climbing fibre responses reduced or abolished the plateau potential, whereas the initial spike-like component of the climbing fibre responses was largely unaffected. Parallel fibre stimulation during already established plateau potentials immediately terminated the plateaus. 3. In distal dendrites parallel fibre stimulation preceding climbing fibre responses reduced or abolished both the plateau potential and the initial component of the climbing fibre responses. Parallel fibre stimulation during established plateau potentials did not immediately terminate the plateau potentials but reduced their duration. 4. The results of the present investigation suggest that single dendritic branches of Purkinje cells serve as independent integrators of mossy fibre and climbing fibre inputs.
Neuroscience Letters, 1984
The present study investigated the duration of afterdepolarizations in Purkinje cell somata following climbing-fibre activation. Intracellular recordings revealed that, in cells with membrane potentials more negative than -50 mV and with normal spike-generating capabilities, climbing-fibre activation resulted in somatic responses with short afterdepolarizations. As the cell deteriorated and the resting membrane potential became more positive, the duration and form of the climbing-fibre response resembled the plateau potentials recorded from proximal dendrites. The absence of plateau potentials in undamaged Purkinje cell somata was confirmed by extracellular recording of test spike amplitudes following evoked climbing-fibre responses.
Neuroscience Letters, 1981
Electrical stimulation has been used to activate climbing fibres (CFs) projecting to the cat cerebeilar cortex, and the effects of low frequency (up to l0 Hz) trains of CF inputs on the discharges of cerebellar cortical neurones has been examined. Repetitive activation of the CF innervating a Purkinie (P) cell could reduce or completely suppress the ongoing simple spike discharges (SS) of the P ceil. Suppression of SS was very readily produced by trains of short bursts of impulses in the CF. SS could remain suppressed for up to 4 min after such a train of CF impulses. Recordings obtained from Golgi, basket and granule cells indicated that these cortical neurones did not mediate the suppression. It is proposed that the SS are suppressed as the result of a direct action of CF impulses on the P cell's dendritic tree which blocks the ongoing transmission of excitation from parallel fibres.
The Journal of Physiology, 1986
1. Extracellularly recorded climbing fibre responses in Purkinje cell somata in the cerebellar cortex were investigated in cats deeply anaesthetized with barbiturate. The effects on the amplitude of initial and secondary spikes of (a) preceding climbing fibre activation, (b) on-beam parallel fibre activation and (c) off-beam parallel fibre activation were studied. 2. When a climbing fibre response was preceded by climbing fibre activation there was a decrease in the amplitude of the initial spike of the second response at intervals up to 25 ms and little effect at longer intervals. Secondary spike amplitude was greatly increased at intervals up to 100 ms. 3. When a complex spike was preceded by on-beam parallel fibre activation there was a decrease in the initial spike amplitude at short intervals and an increase in the amplitude at long intervals. Secondary spike amplitude was increased up to 150 ms after an on-beam parallel fibre volley. 4. When a complex spike was preceded by off-beam parallel fibre stimulation there was an increase in initial spike amplitude at intervals up to about 200 ms and a decrease in secondary spike amplitude at intervals up to about 150 ms. 5. The results show that the amplitude of the secondary spikes can be modified by a preceding input to the Purkinje cell. The results also suggest that the secondary spikes are generated in the Purkinje cell dendrites and the initial spike in the soma.
Dendritic spikes mediate negative synaptic gain control in cerebellar Purkinje cells
Proceedings of the National Academy of Sciences, 2010
Dendritic spikes appear to be a ubiquitous feature of dendritic excitability. In cortical pyramidal neurons, dendritic spikes increase the efficacy of distal synapses, providing additional inward current to enhance axonal action potential (AP) output, thus increasing synaptic gain. In cerebellar Purkinje cells, dendritic spikes can trigger synaptic plasticity, but their influence on axonal output is not well understood. We have used simultaneous somatic and dendritic patch-clamp recordings to directly assess the impact of dendritic calcium spikes on axonal AP output of Purkinje cells. Dendritic spikes evoked by parallel fiber input triggered brief bursts of somatic APs, followed by pauses in spiking, which cancelled out the extra spikes in the burst. As a result, average output firing rates during trains of input remained independent of the input strength, thus flattening synaptic gain. We demonstrate that this "clamping" of AP output by the pause following dendritic spikes is due to activation of high conductance calcium-dependent potassium channels by dendritic spikes. Dendritic spikes in Purkinje cells, in contrast to pyramidal cells, thus have differential effects on temporally coded and rate coded information: increasing the impact of transient parallel fiber input, while depressing synaptic gain for sustained parallel fiber inputs. cerebellum | patch clamp | dendrite | synaptic integration A hallmark of active dendrites is their ability to produce regenerative events known as dendritic spikes (1-8). In pyramidal neurons, the inward currents associated with dendritic spikes provide a strong local depolarization that can boost distal synaptic inputs and enhance their effect on axonal action potential (AP) output (1-4), particularly during burst generation (5, 6). Furthermore, dendritic spikes can enhance the precision of axonal APs in hippocampal pyramidal neurons (7) as well as in neocortical pyramidal cells in vivo (8). Dendritic spikes thus have a boosting effect on the output of pyramidal cells, thus enhancing the gain of the synaptic input-output (I/O) function (9, 10). In contrast, the effect of dendritic spikes on AP output in Purkinje cells is not well understood. Purkinje cell dendritic spikes, originally discovered in alligator Purkinje cells (11, 12), can be triggered by strong parallel fiber (PF) activation (11, 13) or climbing fiber activation (14, 15) and are due solely to activation of dendritic voltage-gated calcium channels (13, 16-18), because Purkinje cells lack dendritic voltage-gated sodium channels and active backpropagation of APs (17,. Calcium influx driven by dendritic spikes has an important role in triggering synaptic plasticity (20-22) and dendritic release of neurotransmitters and neuromodulators (13, 23, 24). Dendritic spikes triggered by climbing fiber input have virtually no effect on the somatic complex spike waveform, probably due to the large synaptic and intrinsic conductances activated during the complex spike (14). However, the functional role of parallel fiber-driven dendritic spikes in regulating axonal output has not been addressed directly. This distinction is crucial, because the state of the Purkinje cell dendritic tree is very different during climbing fiber and parallel fiber excitation (25), and because climbing fiber input occurs only at ≈1 Hz in vivo (26, 27), whereas parallel fiber input occurs continuously at high rates. We have therefore directly probed the relationship between dendritic spikes and axonal AP output in Purkinje cells by using simultaneous dendritic and somatic whole-cell recordings. Our results show that a dendritic spike transiently increases synaptic efficacy by promoting short bursts of somatic APs but dampen AP output over longer timescales. The interplay between these two effects during sustained parallel fiber input results in a "clamping" of Purkinje cells output over long timescales and, thus, a flattening of synaptic gain, in striking contrast to pyramidal cells (9).
Repetitive firing of rat cerebellar parallel fibres after a single stimulation
The Journal of Physiology, 2004
The excitatory postsynaptic currents (EPSCs) evoked in Purkinje cells (PCs) by stimulating parallel fibres (PFs) usually show a single peak, but EPSCs with multiple peaks (polyphasic EPSCs) can be observed in slices from animals older than 15 days. The EPSCs remain polyphasic when the postsynaptic current is reduced (either by reducing the intensity of the PF stimulation or by adding AMPA receptor antagonists) and when the PC membrane potential is made positive. Thus the late peaks are not due to postsynaptic active currents generated in the imperfectly clamped PC, and must arise from repetitive action potentials in the PF. Extracellular recordings from granule cell (GC) somata showed that a single PF stimulation can elicit a doublet or a train of action potentials. Both the late action potentials recorded in the GCs and the late peaks of the polyphasic EPSCs recorded in the PCs were reduced or abolished by paired-pulse stimulation of the PF or by bath application of the GABA A agonist muscimol. The late action potentials in the GCs were also suppressed by local application of muscimol around the cell body. We propose that after a single stimulation of a PF, the antidromic invasion of the ascending axon and the granule cell can trigger a doublet or a burst of action potentials which back-propagate into the PF (except for the first, which finds the PF still in its refractory period). The repetitive activation of the PF by a single stimulation could play a role in the induction of long-term depression.
Excitatory synaptic responses in turtle cerebellar Purkinje cells
The Journal of Physiology, 1989
1. Climbing fibre responses (CFRs) and parallel fibre responses (PFRs) in Purkinje cells have been analysed in intracellular recordings obtained at various levels from cell body to terminal dendrites in the turtle cerebellum in vitro. 2. With increasing stimulus intensity, the PFR recorded in distal dendrites displayed an early regenerative component which was graded at rest and at hyperpolarized membrane potentials, but was all-or-none at depolarized membrane potentials. 3. The all-or-none component had the same characteristics as Ca2" spikes triggered by passing depolarizing current thr®ugh the recording electrode. 4. The repolarizing phase of the PFR had a fast component enhanced by depolarization and diminished by hyperpolarization. 5. In the mid-molecular layer the PFR also included a plateau component which was increasingly prolonged by depolarization and abolished by hyperpolarization. 6. CFRs recorded in the soma had a plateau component, prolonged by local depolarization and abolished by local hyperpolarization. 7. The CFR in distal dendrites included a regenerative component. In some cells this component appeared in an all-or-none manner with local depolarization. In other cells it was smoothly graded with local polarization. 8. In mid-molecular records the CFR was prolonged by local depolarization and presumably electrotonically affected by the configuration of the response more distally and proximally in the cell. 9. It is concluded that excitatory synaptic responses in Purkinje cells include a regenerative Ca21-mediated spike component in the spiny dendrites and a plateau component located in the proximal dendrites and/or the cell body. It is shown that both responses are modulated in configuration by the local membrane potential. In the spiny dendrites activation and inactivation of the transient hyperpolarizing potential appear to govern the Ca2+ influx during the CFR.
Long-Term Depression of the Cerebellar Climbing Fiber–Purkinje Neuron Synapse
Neuron, 2000
first 3 weeks of postnatal life in the rat, an activity-Baltimore, Maryland 21205 dependent refinement occurs such that each Purkinje † Department of Anatomy neuron receives a single CF (Cré pel et al., 1976; Lohof Erasmus University Rotterdam et al., 1996), which is nonetheless extremely powerful, 3000 DR, Rotterdam as it comprises 0051ف release sites (Strata and Rossi, The Netherlands 1998). Activation of the CF leads to a stereotyped membrane response in the Purkinje neuron, which has an all-or-none character (Eccles et al., 1966). These so-Summary called "complex spikes" result from an AMPA receptormediated depolarization, thereby initiating Na ϩ action In classic Marr-Albus-Ito models of cerebellar funcpotentials in the axon that spread passively into the tion, coactivation of the climbing fiber (CF) synapse, dendritic tree (Stuart and Hä usser, 1994). The somatic which provides massive, invariant excitation of Pur-Na ϩ spikes are followed by a series of diminishing spikekinje neurons (coding the unconditioned stimulus), tolets produced mainly by dendritic Ca 2ϩ influx (Lliná s and Sugimori, 1980a, 1980b). In contrast to the CFs, parallel gether with a graded parallel fiber synaptic array (codfibers, which are the axons of cerebellar granule neuing the conditioned stimulus) leads to long-term rons, each make contact with many Purkinje neurons. depression (LTD) of parallel fiber-Purkinje neuron syn-Due to the vast numbers of granule neurons, and their apses, underlying production of a conditioned redivergent input to Purkinje neurons (each receives sponse. Here, we show that the supposedly invariant 000,002ف parallel fiber contacts), this synapse is the CF synapse can also express LTD. Brief 5 Hz stimulamost abundant in the vertebrate central nervous system. tion of the CF resulted in a sustained depression of Activation of single parallel fibers also produces depo-CF EPSCs that did not spread to neighboring parallel larization mediated by AMPA receptors, but this depofiber synapses. Like parallel fiber LTD, CF LTD required larization is typically small and thereby contributes to postsynaptic Ca 2؉ elevation, activation of group 1 the overall rate of Na ϩ spiking (called "simple spiking"). mGluRs, and activation of PKC. CF LTD is potentially Beginning in the 1960s, models of cerebellar network relevant for models of cerebellar motor control and function have suggested that the parallel fiber-Purkinje learning and the developmental conversion from multineuron synapse might be modifiable in a use-dependent ple to single CF innervation of Purkinje neurons. fashion, and that such plasticity might underlie certain forms of motor learning. In these models proposed by
Repetitive firing of cerebellar Purkinje cells in response to impulses in climbing fibre afferents
Neuroscience Letters, 1981
The effects of climbing fibre (CF) impulses on the discharges of cerebellar cortical cells has been studied in the cat. It was found that a brief burst of impulses in a CF can evoke a prolonged excitatory response in the Purkinje (P) cell it innervates. The response consisted of a burst of action potentials that lasted from 50 to 400 msec in different P cells. Bursts of CF impulses were not observed to accelerate the discharges of granule ceils. It is therefore suggested that this powerful response results from a direct action of CF impulses on the P cell.
Spread of synaptic activity along parallel fibres in cat cerebellar anterior lobe
Experimental Brain Research, 1992
1. Mossy fibre evoked activity in the cerebellar cortex elicited by peripheral electrical stimulation was studied in chloralose anesthetized cats. The distribution of intracortical field potentials in the C3 and D zones was mapped in order to determine if there is a spread of synaptic activity outside the mossy fibre termination area. This area was identified by the presence of short latency synaptic field potentials in the granular layer. 2. Molecular layer field potentials were recorded up to 1.5 mm outside the mossy fibre termination area. The latencies of these potentials increased with increasing distance from the mossy fibre termination area, corresponding to a conduction velocity of about 0.4 m/s. 3. Recordings from Purkinje cells, within and outside the mossy fibre termination area, revealed an increase of simple spike activity at latencies corresponding to those of the field potentials in the same location. 4. From the spatial and temporal characteristics of the evoked activity, it is concluded that a mossy fibre input results in spread of synaptic activity along the parallel fibres. 5. The findings are discussed in relation to the recently discovered microzonal organization of the C3 zone. It is proposed that the organization of this zone offers a possibility for the control of muscle synergies, each synergy being represented by a mossy fibre input and the specific set of microzones activated by this input via the parallel fibres.