Molecular frequency filters at central synapses

Thomson, Alex M.

doi:10.1016/s0301-0082(00)00008-3

Cited by 130 publications

(108 citation statements)

References 198 publications

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“…59) is the firing-frequency tunability of the pyramidal cell-interneuron synapse (23,(46)(47)(48) and their low-discharge threshold (26,27). Furthermore, soma targeting interneurons are endowed with resonant properties that allow them to respond maximally when presynaptic neurons fire in the ␥-frequency range (23,34), whereas dendrite-targeting interneurons respond best at frequency (49,50).…”

Section: Distance Representation By Time Compression Is Speed-dependentmentioning

confidence: 99%

Hippocampal place cell assemblies are speed-controlled oscillators

Geisler

Robbe

Zugaro

et al. 2007

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

253

321

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The phase of spikes of hippocampal pyramidal cells relative to the local field oscillation shifts forward (''phase precession'') over a full cycle as the animal crosses the cell's receptive field (''place field''). The linear relationship between the phase of the spikes and the travel distance within the place field is independent of the animal's running speed. This invariance of the phase-distance relationship is likely to be important for coordinated activity of hippocampal cells and space coding, yet the mechanism responsible for it is not known. Here we show that at faster running speeds place cells are active for fewer cycles but oscillate at a higher frequency and emit more spikes per cycle. As a result, the phase shift of spikes from cycle to cycle (i.e., temporal precession slope) is faster, yet spatial-phase precession stays unchanged. Interneurons can also show transient-phase precession and contribute to the formation of coherently precessing assemblies. We hypothesize that the speed-correlated acceleration of place cell assembly oscillation is responsible for the phase-distance invariance of hippocampal place cells.cell assembly ͉ interneurons ͉ phase locking ͉ phase precession ͉ oscillations W hile animals navigate in an environment, the hippocampal local field potential (LFP) is characterized by a highly regular oscillation (8-10 Hz). Principal cells in the hippocampus show place-specific firing by two criteria. First, the firing is tuned to a particular location (''place field''), showing a bellshaped tuning curve centered around its preferred location (1). Second, the timing of spikes within subsequent cycles systematically shifts forward (''phase precession''), Ϸ1 full cycle in total, as the rat runs through the place field of the neuron (2, 3) (see also Fig. 1 A and B). Both the firing rate and discharge phase within a cycle are correlated with the rat's position. However, how the rate change and -phase precession of spikes are related is poorly understood. The available experiments support both a rate-phase interdependence (4-6) and independence (7).Several explanations for the place-phase relationship were put forward (4)(5)(6)(8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18). To confront these models, we examined the relationship among running speed, oscillation frequency of place cells and LFP , and timing of spikes within the cycle. We show that principal cells oscillate at a frequency faster than the simultaneously recorded LFP oscillation, and that this oscillation frequency depends on the rat's running speed. Together with the place-and speed-dependent oscillation frequencies of interneurons, the findings support the hypothesis that place coding results from coordinated network activity. We propose that the locomotion speed-dependent oscillation of place cell assemblies may underlie the mechanisms responsible for distance encoding in the hippocampus. ResultsWe recorded the firing patterns of pyramidal cells, interneurons, and the LFP from the CA1 pyramidal layer of rats as they ran on a U-shap...

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Section: Distance Representation By Time Compression Is Speed-dependentmentioning

confidence: 99%

Hippocampal place cell assemblies are speed-controlled oscillators

Geisler

Robbe

Zugaro

et al. 2007

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

253

321

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“…S ynaptic strength within neuronal circuits is continuously modified because of short-term plasticity (STP) (1)(2)(3)(4)(5). STP bestows circuits with functional capabilities such as detection of sudden changes, filtering, and fidelity transfer (5)(6)(7)(8).…”

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confidence: 99%

“…STP bestows circuits with functional capabilities such as detection of sudden changes, filtering, and fidelity transfer (5)(6)(7)(8). Short-term depression (STD) is a form of STP.…”

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confidence: 99%

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Dopaminergic modulation of short-term synaptic plasticity at striatal inhibitory synapses

Tecuapetla

Carrillo-Reid

Bargas

et al. 2007

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

123

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“…Rather, such short-term plasticity plays an essential role in determining the cut-off frequency of a synapse, thus limiting the content of information flow at a specific pathway [32,30,42-45]. The most important consequences of the higher PPR of type I DMX neurons are that these neurons are capable of being activated by repeated high-frequency afferent inputs up to a few tens of Hz in a manner that contrasts with that of the dm-cNTS and type II DMX neurons that filter out high-frequency components and can be sufficiently excited only by low (~0.1 Hz) frequency inputs.…”

Section: Discussionmentioning

confidence: 99%

Distinct target cell-dependent forms of short-term plasticity of the central visceral afferent synapses of the rat

et al. 2010

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Background The visceral afferents from various cervico-abdominal sensory receptors project to the dorsal vagal complex (DVC), which is composed of the nucleus of the solitary tract (NTS), the area postrema and the dorsal motor nucleus of the vagus nerve (DMX), via the vagus and glossopharyngeal nerves and then the solitary tract (TS) in the brainstem. While the excitatory transmission at the TS-NTS synapses shows strong frequency-dependent suppression in response to repeated stimulation of the afferents, the frequency dependence and short-term plasticity at the TS-DMX synapses, which also transmit monosynaptic information from the visceral afferents to the DVC neurons, remain largely unknown. Results Recording of the EPSCs activated by paired or repeated TS stimulation in the brainstem slices of rats revealed that, unlike NTS neurons whose paired-pulse ratio (PPR) is consistently below 0.6, the distribution of the PPR of DMX neurons shows bimodal peaks that are composed of type I (PPR, 0.6-1.5; 53% of 120 neurons recorded) and type II (PPR, < 0.6; 47%) neurons. Some of the type I DMX neurons showed paired-pulse potentiation. The distinction of these two types depended on the presynaptic release probability and the projection target of the postsynaptic cells; the distinction was not dependent on the location or soma size of the cell, intensity or site of the stimulation, the latency, standard deviation of latency or the quantal size. Repeated stimulation at 20 Hz resulted in gradual and potent decreases in EPSC amplitude in the NTS and type II DMX neurons, whereas type I DMX neurons displayed only slight decreases, which indicates that the DMX neurons of this type could be continuously activated by repeated firing of primary afferent fibers at a high (~10 Hz) frequency. Conclusions These two general types of short-term plasticity might contribute to the differential activation of distinct vago-vagal reflex circuits, depending on the firing frequency and type of visceral afferents.

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Molecular frequency filters at central synapses

Cited by 130 publications

References 198 publications

Hippocampal place cell assemblies are speed-controlled oscillators

Hippocampal place cell assemblies are speed-controlled oscillators

Dopaminergic modulation of short-term synaptic plasticity at striatal inhibitory synapses

Distinct target cell-dependent forms of short-term plasticity of the central visceral afferent synapses of the rat

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