scholarly journals Unusually slow spike frequency adaptation in deep cerebellar nuclei neurons preserves linear transformations on the sub-second time scale

2021 ◽  
Author(s):  
Mehak M Khan ◽  
Christopher H Chen ◽  
wade G regehr
Keyword(s):  
Brain Slices ◽  
Cerebellar Nuclei ◽  
Spike Frequency ◽  
Initial Increase ◽  
Projection Neurons ◽  
Spike Frequency Adaptation ◽  
Linear Transformations ◽  
Deep Cerebellar Nuclei ◽  
Frequency Adaptation

Purkinje cells (PCs) are spontaneously active neurons of the cerebellar cortex that inhibit glutamatergic projection neurons within the deep cerebellar nuclei (DCN) that in turn provide the primary cerebellar output. Brief reductions in PC firing rapidly increase DCN neuron firing. However, prolonged reductions in PC inhibition, as seen in some disease states, certain types of transgenic mice, and in acute slices of the cerebellum, do not evoke large sustained increases in DCN firing. Here we test whether there is a mechanism of spike-frequency adaptation in DCN neurons that could account for these properties. We find that prolonged optogenetic suppression of PC synapses in vivo transiently elevates PC firing that strongly adapts within ten seconds. We perform current-clamp recordings at near physiological temperature in acute brain slices to examine how DCN neurons respond to prolonged depolarizations. Adaptation in DCN neurons is exceptionally slow and bidirectional. A depolarizing current step evokes large initial increases in firing that decay to less than 20% of the initial increase within approximately ten seconds. Such slow adaptation could allow DCN neurons to adapt to prolonged changes in PC firing while maintaining their linear firing frequency-current relationship on subsecond time scales.

Morphological and Electrophysiological Properties of Principal Neurons in the Rat Lateral Amygdala In Vitro

2001 ◽  
Vol 85 (2) ◽  
pp. 714-723 ◽  
Author(s):  
E.S.L. Faber ◽  
R. J. Callister ◽  
P. Sah
Keyword(s):  
Cell Morphology ◽  
Brain Slices ◽  
Spike Trains ◽  
Spike Frequency ◽  
Morphological Properties ◽  
Spike Frequency Adaptation ◽  
Differential Distribution ◽  
Lateral Amygdala ◽  
Frequency Adaptation ◽  
Firing Properties

In this study, we characterize the electrophysiological and morphological properties of spiny principal neurons in the rat lateral amygdala using whole cell recordings in acute brain slices. These neurons exhibited a range of firing properties in response to prolonged current injection. Responses varied from cells that showed full spike frequency adaptation, spiking three to five times, to those that showed no adaptation. The differences in firing patterns were largely explained by the amplitude of the afterhyperpolarization (AHP) that followed spike trains. Cells that showed full spike frequency adaptation had large amplitude slow AHPs, whereas cells that discharged tonically had slow AHPs of much smaller amplitude. During spike trains, all cells showed a similar broadening of their action potentials. Biocytin-filled neurons showed a range of pyramidal-like morphologies, differed in dendritic complexity, had spiny dendrites, and differed in the degree to which they clearly exhibited apical versus basal dendrites. Quantitative analysis revealed no association between cell morphology and firing properties. We conclude that the discharge properties of neurons in the lateral nucleus, in response to somatic current injections, are determined by the differential distribution of ionic conductances rather than through mechanisms that rely on cell morphology.

scholarly journals Selective attenuation of Ether-a-go-go related K+ currents by endogenous acetylcholine reduces spike-frequency adaptation and network correlation

eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Edward D Cui ◽  
Ben W Strowbridge
Keyword(s):  
Late Phase ◽  
Pyramidal Cells ◽  
Spike Frequency ◽  
Spike Frequency Adaptation ◽  
Firing Rates ◽  
Frequency Adaptation ◽  
Rat Neocortex ◽  
Persistent Firing ◽  
K Current

Most neurons do not simply convert inputs into firing rates. Instead, moment-to-moment firing rates reflect interactions between synaptic inputs and intrinsic currents. Few studies investigated how intrinsic currents function together to modulate output discharges and which of the currents attenuated by synthetic cholinergic ligands are actually modulated by endogenous acetylcholine (ACh). In this study we optogenetically stimulated cholinergic fibers in rat neocortex and find that ACh enhances excitability by reducing Ether-à-go-go Related Gene (ERG) K+ current. We find ERG mediates the late phase of spike-frequency adaptation in pyramidal cells and is recruited later than both SK and M currents. Attenuation of ERG during coincident depolarization and ACh release leads to reduced late phase spike-frequency adaptation and persistent firing. In neuronal ensembles, attenuating ERG enhanced signal-to-noise ratios and reduced signal correlation, suggesting that these two hallmarks of cholinergic function in vivo may result from modulation of intrinsic properties.

scholarly journals Slow Spike Frequency Adaptation in Neurons of the Rat Subthalamic Nucleus

2009 ◽  
Vol 102 (6) ◽  
pp. 3689-3697 ◽  
Author(s):  
David Barraza ◽  
Hitoshi Kita ◽  
Charles J. Wilson
Keyword(s):  
Firing Rate ◽  
Subthalamic Nucleus ◽  
Similar Rate ◽  
Excitatory Input ◽  
Spike Frequency ◽  
Spike Frequency Adaptation ◽  
Frequency Adaptation ◽  
Long Duration ◽  
Subthalamic Neurons

Neurons of the subthalamic nucleus (STN) are very sensitive to applied currents, firing at 10–20/s during spontaneous activity, but increasing to peak firing rates of 200/s with applied currents <0.5 nA. They receive a powerful tonic excitatory input from neurons in the cerebral cortex, yet in vivo maintain an irregular firing rate only slightly higher than the autonomous firing rate seen in slices. Spike frequency adaptation acts to normalize background firing rate by removing slow trends in firing due to changes in average input. Subthalamic neurons have been previously described as showing little spike frequency adaptation, but this was based on tests using brief stimuli. We applied long-duration depolarizing current steps to STN neurons in slices and observed a very strong spike frequency adaptation with a time constant of 20 s and that recovered at a similar rate. This adaptation could return firing to near-baseline levels during prolonged current pulses that transiently drove the cells at high rates. The current responsible for adaptation was studied in voltage clamp during and after high-frequency driving of the cell and was determined to be a slowly accumulating K+ current. This current was independent of calcium or sodium entry and could be induced with long-duration voltage steps after blockade of action potentials. In addition to the adaptation current, driven firing produced slow inactivation of the persistent Na+ current, which also contributed to the reduced excitability of STN cells during and after driven firing.

Electrophysiological Classes of Cat Primary Visual Cortical Neurons In Vivo as Revealed by Quantitative Analyses

2003 ◽  
Vol 89 (3) ◽  
pp. 1541-1566 ◽  
Author(s):  
Lionel G. Nowak ◽  
Rony Azouz ◽  
Maria V. Sanchez-Vives ◽  
Charles M. Gray ◽  
David A. McCormick
Keyword(s):  
Short Duration ◽  
Cortical Neurons ◽  
Action Potentials ◽  
Low Frequency ◽  
Pyramidal Cells ◽  
Spike Frequency ◽  
Spike Frequency Adaptation ◽  
Frequency Adaptation ◽  
Layer 4

To facilitate the characterization of cortical neuronal function, the responses of cells in cat area 17 to intracellular injection of current pulses were quantitatively analyzed. A variety of response variables were used to separate the cells into subtypes using cluster analysis. Four main classes of neurons could be clearly distinguished: regular spiking (RS), fast spiking (FS), intrinsic bursting (IB), and chattering (CH). Each of these contained significant subclasses. RS neurons were characterized by trains of action potentials that exhibited spike frequency adaptation. Morphologically, these cells were spiny stellate cells in layer 4 and pyramidal cells in layers 2, 3, 5, and 6. FS neurons had short-duration action potentials (<0.5 ms at half height), little or no spike frequency adaptation, and a steep relationship between injected current intensity and spike discharge frequency. Morphologically, these cells were sparsely spiny or aspiny nonpyramidal cells. IB neurons typically generated a low frequency (<425 Hz) burst of spikes at the beginning of a depolarizing current pulse followed by a tonic train of action potentials for the remainder of the pulse. These cells were observed in all cortical layers, but were most abundant in layer 5. Finally, CH neurons generated repetitive, high-frequency (350–700 Hz) bursts of short-duration (<0.55 ms) action potentials. Morphologically, these cells were layer 2–4 (mainly layer 3) pyramidal or spiny stellate neurons. These results indicate that firing properties do not form a continuum and that cortical neurons are members of distinct electrophysiological classes and subclasses.

scholarly journals Spike Frequency Adaptation and Neocortical Rhythms

2002 ◽  
Vol 88 (2) ◽  
pp. 761-770 ◽  
Author(s):  
Galit Fuhrmann ◽  
Henry Markram ◽  
Misha Tsodyks
Keyword(s):  
Firing Rate ◽  
Pyramidal Neurons ◽  
Spike Frequency ◽  
Spike Frequency Adaptation ◽  
Patch Clamp Technique ◽  
Response Characteristics ◽  
Frequency Adaptation ◽  
Whole Cell Patch Clamp ◽  
The Mean

Spike-frequency adaptation in neocortical pyramidal neurons was examined using the whole cell patch-clamp technique and a phenomenological model of neuronal activity. Noisy current was injected to reproduce the irregular firing typically observed under in vivo conditions. The response was quantified by computing the poststimulus histogram (PSTH). To simulate the spiking activity of a pyramidal neuron, we considered an integrate-and-fire model to which an adaptation current was added. A simplified model for the mean firing rate of an adapting neuron under noisy conditions is also presented. The mean firing rate model provides a good fit to both experimental and simulation PSTHs and may therefore be used to study the response characteristics of adapting neurons to various input currents. The models enable identification of the relevant parameters of adaptation that determine the shape of the PSTH and allow the computation of the response to any change in injected current. The results suggest that spike frequency adaptation determines a preferred frequency of stimulation for which the phase delay of a neuron's activity relative to an oscillatory input is zero. Simulations show that the preferred frequency of single neurons dictates the frequency of emergent population rhythms in large networks of adapting neurons. Adaptation could therefore be one of the crucial factors in setting the frequency of population rhythms in the neocortex.

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

2003 ◽  
Vol 89 (4) ◽  
pp. 1738-1747 ◽  
Author(s):  
Carlos D. Aizenman ◽  
Eric J. Huang ◽  
David J. Linden
Keyword(s):  
Electrical Properties ◽  
Brain Slices ◽  
Cerebellar Nuclei ◽  
Neuronal Morphology ◽  
Intrinsic Excitability ◽  
Projection Neurons ◽  
Electrical Excitability ◽  
Deep Cerebellar Nuclei ◽  
Younger Age ◽  
Large Projection

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.

Slow Adaptation in Fast-Spiking Neurons of Visual Cortex

2005 ◽  
Vol 93 (2) ◽  
pp. 1111-1118 ◽  
Author(s):  
V. F. Descalzo ◽  
L. G. Nowak ◽  
J. C. Brumberg ◽  
D. A. McCormick ◽  
M. V. Sanchez-Vives
Keyword(s):  
Time Scale ◽  
Time Course ◽  
Firing Frequency ◽  
Spike Frequency ◽  
Spike Frequency Adaptation ◽  
Slow Time ◽  
Frequency Adaptation ◽  
Slow Adaptation ◽  
Fast Spiking

Fast-spiking (FS) neurons are a class of inhibitory interneurons classically characterized as having short-duration action potentials (<0.5 ms at half height) and displaying little to no spike-frequency adaptation during short (<500 ms) depolarizing current pulses. As a consequence, the resulting injected current intensity versus firing frequency relationship is typically steep, and they can achieve firing frequencies of ≤1 kHz. Here we have investigated the properties of FS neurons discharges on a longer time scale. Twenty second discharges were induced in electrophysiologically identified FS neurons by means of current injection either with sinusoidal current or with square pulses. We found that virtually all FS neurons recorded in cortical slices do show spike-frequency adaptation but with a slow time course (τ = 2–19 s). This slow time course has precluded the observation of this property in previous studies that used shorter pulses. Contrary to the classical view of FS neurons functional properties, long-duration discharges were followed by a slow afterhyperpolarization lasting ≤23 s. During this postadaptation period, the excitability of the neurons was decreased on average for 16.7 ± 6.8 s, therefore rendering the cell less responsive to subsequent afferent inputs. Slow adaptation is also reported here for FS neurons recorded in vivo. This longer time scale of adaptation in FS neurons may be critical for balancing excitation and inhibition as well as for the understanding of cortical network computations.

scholarly journals Spike-Frequency Adaptation and Intrinsic Properties of an Identified, Looming-Sensitive Neuron

2006 ◽  
Vol 96 (6) ◽  
pp. 2951-2962 ◽  
Author(s):  
Fabrizio Gabbiani ◽  
Holger G. Krapp
Keyword(s):  
Time Course ◽  
Input Resistance ◽  
Spike Frequency ◽  
Membrane Properties ◽  
Inward Rectification ◽  
Movement Detector ◽  
Spike Frequency Adaptation ◽  
Current Pulses ◽  
Frequency Adaptation

We investigated in vivo the characteristics of spike-frequency adaptation and the intrinsic membrane properties of an identified, looming-sensitive interneuron of the locust optic lobe, the lobula giant movement detector (LGMD). The LGMD had an input resistance of 4–5 MΩ, a membrane time constant of about 8 ms, and exhibited inward rectification and rebound spiking after hyperpolarizing current pulses. Responses to depolarizing current pulses revealed the neuron's intrinsic bursting properties and pronounced spike-frequency adaptation. The characteristics of adaptation, including its time course, the attenuation of the firing rate, the mutual dependency of these two variables, and their dependency on injected current, closely followed the predictions of a model first proposed to describe the adaptation of cat visual cortex pyramidal neurons in vivo. Our results thus validate the model in an entirely different context and suggest that it might be applicable to a wide variety of neurons across species. Spike-frequency adaptation is likely to play an important role in tuning the LGMD and in shaping the variability of its responses to visual looming stimuli.

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