Stimulus History Reliably Shapes Action Potential Waveforms of Cortical Neurons

Polavieja, Gonzalo G. de; Harsch, Annette; Kleppe, Ingo; Robinson, Hugh P. C.; Juusola, Mikko

doi:10.1523/jneurosci.0242-05.2005

Cited by 69 publications

(82 citation statements)

References 35 publications

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“…In addition to discharge rate, the shape of the action potential (Matsumura et al, 1995;de Polavieja et al, 2005;Gold et al, 2006) is also thought to reflect intrinsic changes in neuronal excitability (e.g., availability of sodium channels). We used the From top to bottom, The relationship between the mean corrected firing rate and the frequency of pauses; the relationship between the mean corrected firing rate and the mean pause duration; and the relationship between the mean corrected firing rate and the amount of time the cell was in a pause.…”

Section: Relationships Between Discharge Parameters and Pausesmentioning

confidence: 99%

Statistical Properties of Pauses of the High-Frequency Discharge Neurons in the External Segment of the Globus Pallidus

Elias¹,

Joshua²,

Goldberg³

et al. 2007

J. Neurosci.

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The neurons of many basal ganglia nuclei, including the external and internal globus pallidus (GPe and GPi, respectively) and the substantia nigra pars reticulata (SNr) are characterized by their high-frequency (50 -100 spikes/s) tonic discharge (HFD). However, the high firing rate of GPe neurons is interrupted by long pauses. We studied the extracellularly recorded spiking activity of 212 well-isolated HFD GPe and 52 GPi/SNr neurons from five monkeys during different states of behavioral activity. An algorithm that maximizes the surprise function was used to detect pauses and pauser cells ("pausers"). Only 6% of the GPi/SNr neurons versus as many as 56% of the GPe neurons were classified as pausers. The GPe average pause duration equals 0.62 s. The interpause intervals follow a Poissonian distribution with a frequency of 13 pauses/minute. No linear relationship was found between pause parameters (duration or frequency) and the firing rate of the cell. Pauses were preceded by various changes in firing rate but not dominantly by a decrease. The average amplitude and duration of the spike waveform was modulated only after the pause but not before it. Pauses of pairs of cells that were recorded simultaneously were not correlated. The probability of GPe cells to pause spontaneously was extremely variable among monkeys (30 -90%) and inversely related to the degree of the monkey's motor activity. These findings suggest that spontaneous GPe pauses are related to low-arousal periods and are generated by a process that is independent of the discharge properties of the cells.

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Section: Relationships Between Discharge Parameters and Pausesmentioning

confidence: 99%

Statistical Properties of Pauses of the High-Frequency Discharge Neurons in the External Segment of the Globus Pallidus

Elias¹,

Joshua²,

Goldberg³

et al. 2007

J. Neurosci.

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“…Action potential broadening is much more pronounced in mossy fiber boutons than in the calyx of Held in the auditory brainstem [11], implying that broadening is a specific property of cortical presynaptic terminals. This may suggest that information in the mossy fiber system is not only coded by action potential frequency and timing but also as action potential duration [25]. Second, recent experiments revealed that subthreshold excitatory postsynaptic potentials (EPSPs) can be passively propagated from the somatodendritic domain of granule cells to mossy fiber boutons [2].…”

Section: Abstract Presynaptic Recording Mossy Fiber Boutons Mossymentioning

confidence: 99%

Timing and efficacy of transmitter release at mossy fiber synapses in the hippocampal network

Bischofberger

Engel

Frotscher

et al. 2006

Pflugers Arch - Eur J Physiol

114

110

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It is widely accepted that the hippocampus plays a major role in learning and memory. The mossy fiber synapse between granule cells in the dentate gyrus and pyramidal neurons in the CA3 region is a key component of the hippocampal trisynaptic circuit. Recent work, partially based on direct presynaptic patch-clamp recordings from hippocampal mossy fiber boutons, sheds light on the mechanisms of synaptic transmission and plasticity at mossy fiber synapses. A high Na + channel density in mossy fiber boutons leads to a large amplitude of the presynaptic action potential. Together with the fast gating of presynaptic Ca 2+ channels, this generates a large and brief presynaptic Ca 2+ influx, which can trigger transmitter release with high efficiency and temporal precision. The large number of release sites, the large size of the releasable pool of vesicles, and the huge extent of presynaptic plasticity confer unique strength to this synapse, suggesting a large impact onto the CA3 pyramidal cell network under specific behavioral conditions. The characteristic properties of the hippocampal mossy fiber synapse may be important for pattern separation and information storage in the dentate gyrus-CA3 cell network.Keywords Presynaptic recording . Mossy fiber boutons . Mossy fiber synapses . Hippocampus . Autoassociative networks . Episodic memory . Synaptic efficacyThe mossy fiber synapse: a key connection in the hippocampal networkThe hippocampal formation consists of three types of principal neurons: granule cells in the dentate gyrus, CA3 pyramidal cells, and CA1 pyramidal neurons. These cells are interconnected by glutamatergic synapses, forming the classical trisynaptic circuit (Fig. 1a,b). Dentate gyrus granule cells receive excitatory glutamatergic input from layer 2 pyramidal cells of the entorhinal cortex and project to CA3 pyramidal cells. CA3 pyramidal cells project to CA1 cells, which in turn project to the subiculum and back to the entorhinal cortex [4]. In addition to this trisynaptic circuit, there is also a direct input from the entorhinal cortex to both CA3 and CA1 pyramidal cells. Furthermore, CA3 pyramidal neurons are extensively connected to each other via recurrent collateral synapses.The nonmyelinated axons of the granule cells, the socalled mossy fibers, show several structural properties that distinguish them from the other synaptic pathways [39]. They project to the CA3 region, mainly traveling within a narrow band termed "stratum lucidum." Several (∼15) large "giant" boutons (∼3-5-μm diameter) emerge from a single mossy fiber axon, either arranged in an en passant manner or attached to the main axon via a short perpendicular axonal branch [1,8,29,31] (Fig. 1c,d). A large mossy fiber bouton typically contacts only a single CA3 pyramidal neuron [21], and a mossy fiber axon contacts a given CA3 pyramidal neuron only once, as boutons are ∼150 μm apart. As the rat hippocampus contains ∼1 million granule cells

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“…Mostly in invertebrates, for example in leech segmental ganglia, crustacean stomatogastric ganglia or in insect visual pathways, but also in vertebrate nervous systems, neurons are known that convey information by signals that combine graded potential shifts with spikes of variable amplitude, termed in the following "mixed potential signals" (e.g. Hengstenberg, 1977;Graubard et al, 1980;Simmons, 1982;Arbas and Calabrese, 1987;Juusola et al, 1995;Awatramani et al, 2005;de Polavieja et al, 2005;Alle and Geiger, 2006;Shu et al, 2006;Juusola et al, 2007). It is tantalizing to suggest that coarse information (analogous to spike rate) may be carried by the graded component while temporally precise information is present in the timing of spikes of these mixed potential neurons.…”

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confidence: 99%

“…A combination of graded and spike-like signals in the axonal membrane potential has been shown to maximize information transmission (Haag and Borst, 1998;de Polavieja et al, 2005;Juusola et al, 2007).…”

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confidence: 99%

Precise timing in fly motion vision is mediated by fast components of combined graded and spike signals

2009

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Abstract-Firing of an individual neuron is determined by the activity of its presynaptic input ensemble. In this study we analyzed how presynaptic signals with different dynamics interact to control postsynaptic activity. In the blowfly's visual system we simultaneously recorded in vivo from an identified motion-sensitive neuron and from elements of the presynaptic ensemble. The presynaptic cells themselves are mutually electrically coupled and convey both graded and spike signals to their common postsynaptic target. We elicited spikes in the postsynaptic neuron by voltage-clamping one of the presynaptic neurons to various holding potentials and then analyzed the time course of the holding current. Current transients in the clamped presynaptic cell were found to coincide with postsynaptic spikes. The current transients were highly variable in amplitude and occasionally absent during postsynaptic spiking. These characteristics indicate that the current transients in the voltage-clamped neuron result from spikes in electrically coupled co-members of the presynaptic ensemble. Our results suggest that electrical coupling among presynaptic neurons mediates synchronization of spikes within the cell ensemble. Moreover, our findings demonstrate that the graded response component of the presynaptic cells effectively controls the postsynaptic firing rate on a coarse scale while the precise timing of the postsynaptic spikes is a consequence of spikes superimposed on the graded signals of the presynaptic neurons.

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Stimulus History Reliably Shapes Action Potential Waveforms of Cortical Neurons

Cited by 69 publications

References 35 publications

Statistical Properties of Pauses of the High-Frequency Discharge Neurons in the External Segment of the Globus Pallidus

Statistical Properties of Pauses of the High-Frequency Discharge Neurons in the External Segment of the Globus Pallidus

Timing and efficacy of transmitter release at mossy fiber synapses in the hippocampal network

Precise timing in fly motion vision is mediated by fast components of combined graded and spike signals

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