Two Forms of Synaptic Depression Produced by Differential Neuromodulation of Presynaptic Calcium Channels

Burke, Kenneth; Keeshen, Caroline M.; Bender, Kevin J.

doi:10.1016/j.neuron.2018.07.030

Cited by 48 publications

(58 citation statements)

References 95 publications

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“…The similar effects of D1 receptor activation that we observed support the idea that the majority of commissural fibers is targeting layer V. Furthermore, Anastasiades et al () have also reported that D1 receptor activation enhances cortico‐cortical connectivity, supporting the results reported here. Contrary to results reported here, others have shown that D1 receptor activation suppresses commissural fiber‐evoked EPSCs in layer V pyramidal cells through a presynaptic mechanism involving modulation of calcium channels (Burke et al, ). However, these studies were conducted without the presence of GABA blockers, thus likely involving D1 modulatory effects on GABAergic interneurons.…”

Section: Discussioncontrasting

confidence: 99%

Dopaminergic D1 receptor effects on commissural inputs targeting layer V pyramidal subtypes of the mouse medial prefrontal cortex

Leyrer‐Jackson

Thomas

2019

Physiol Rep

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In humans, prefrontal cortical areas are known to support goal‐directed behaviors, mediating a variety of functions that render behavior more flexible in the face of changing environmental demands. In mice, these functions are mediated by homologous regions within medial prefrontal cortex (mPFC) and rely heavily on proper dopaminergic tone. Comprised of two major subtypes, pyramidal tract (PT) and intratelencephalic (IT), layer V pyramidal cells serve as the major outputs of the mPFC, targeting brainstem nuclei and the contralateral hemisphere, respectively. However, it remains relatively unknown how cortical inputs targeting these subtypes are integrated. We explored how layer V pyramidal cell subtypes integrate commissural inputs, which integrate information flow between the hemispheres. An optogenetic approach was used to elicit commissural fiber activation onto PT and IT cells and the effects of D1 receptor activation on elicited EPSPs were explored. We showed that commissural inputs into PT and IT cells elicit facilitating and depressing EPSP patterns, respectively. D1 receptor activation increased the initial EPSP amplitude, enhanced EPSP facilitation, and prolonged EPSP decay time constant in PT cells. In IT cells, D1 receptor activation increased commissural‐evoked initial EPSP amplitude but did not affect facilitation or EPSP shape. Furthermore, D1 receptor activation elicited burst firing in a subset of PT cells in response to commissural fiber activation. Combined, these results lend insight into the role of dopamine in promoting persistent firing and temporal integration in PT and IT cells, respectively, that in turn may contribute to working memory functions.

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Section: Discussioncontrasting

confidence: 99%

Dopaminergic D1 receptor effects on commissural inputs targeting layer V pyramidal subtypes of the mouse medial prefrontal cortex

Leyrer‐Jackson

Thomas

2019

Physiol Rep

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“… 57 Calcium dynamics in the presynaptic terminals are also influenced by neuromodulators such as adenosine 55 and dopamine. 58 …”

Section: Axonal Calcium Signals: As a Proxy For Presynaptic Activitymentioning

confidence: 99%

Interpreting in vivo calcium signals from neuronal cell bodies, axons, and dendrites: a review

2019

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Calcium imaging is emerging as a popular technique in neuroscience. A major reason is that intracellular calcium transients are reflections of electrical events in neurons. For example, calcium influx in the soma and axonal boutons accompanies spiking activity, whereas elevations in dendrites and dendritic spines are associated with synaptic inputs and local regenerative events. However, calcium transients have complex spatiotemporal dynamics, and since most optical methods visualize only one of the somatic, axonal, and dendritic compartments, a straightforward inference of the underlying electrical event is typically challenging. We highlight experiments that have directly calibrated in vivo calcium signals recorded using fluorescent indicators against electrophysiological events. We address commonly asked questions such as: Can calcium imaging be used to characterize neurons with high firing rates? Can the fluorescent signal report a decrease in spiking activity? What is the evidence that calcium transients in subcellular compartments correspond to distinct presynaptic axonal and postsynaptic dendritic events? By reviewing the empirical evidence and limitations, we suggest that, despite some caveats, calcium imaging is a versatile method to characterize a variety of neuronal events in vivo.

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“…; Burke et al . ), the vast majority of studies use concentrations of calcium in the extracellular solution that are higher than physiological levels, between 2 and 4 mM, to support synaptic transmission and suppress intrinsic excitability. In this study, we determine the concentration of ionized calcium in human cerebrospinal fluid (hCSF), and characterize the effects of using physiological (~1.2 mM), as compared to standard (2 mM), artificial cerebrospinal fluid (aCSF) calcium on intrinsic neuronal excitability, synaptic transmission, paired‐pulse plasticity, and long‐term potentiation in rat CA1 pyramidal cells.…”

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confidence: 99%

Ionized calcium in human cerebrospinal fluid and its influence on intrinsic and synaptic excitability of hippocampal pyramidal neurons in the rat

Forsberg

Seth

Björefeldt

et al. 2019

Journal of Neurochemistry

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It is well‐known that the extracellular concentration of calcium affects neuronal excitability and synaptic transmission. Less is known about the physiological concentration of extracellular calcium in the brain. In electrophysiological brain slice experiments, the artificial cerebrospinal fluid traditionally contains relatively high concentrations of calcium (2‐4 mM) to support synaptic transmission and suppress neuronal excitability. Using an ion‐selective electrode, we determined the fraction of ionized calcium in healthy human cerebrospinal fluid to 1.0 mM of a total concentration of 1.2 mM (86%). Using patch‐clamp and extracellular recordings in the CA1 region in acute slices of rat hippocampus, we then compared the effects of this physiological concentration of calcium with the commonly used 2 mM on neuronal excitability, synaptic transmission, and long‐term potentiation (LTP) to examine the magnitude of changes in this range of extracellular calcium. Increasing the total extracellular calcium concentration from 1.2 to 2 mM decreased spontaneous action potential firing, induced a depolarization of the threshold, and increased the rate of both de‐ and repolarization of the action potential. Evoked synaptic transmission was approximately doubled, with a balanced effect between inhibition and excitation. In 1.2 mM calcium high‐frequency stimulation did not result in any LTP, whereas a prominent LTP was observed at 2 or 4 mM calcium. Surprisingly, this inability to induce LTP persisted during blockade of GABAergic inhibition. In conclusion, an increase from the physiological 1.2 mM to 2 mM calcium in the artificial cerebrospinal fluid has striking effects on neuronal excitability, synaptic transmission, and the induction of LTP. Open science badges This article has received a badge for *Open Materials* because it provided all relevant information to reproduce the study in the manuscript. The complete Open Science Disclosure form for this article can be found at the end of the article. More information about the Open Practices badges can be found at https://cos.io/our-services/open-science-badges/. Read the Editorial Highlight for this article on page 435.

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Two Forms of Synaptic Depression Produced by Differential Neuromodulation of Presynaptic Calcium Channels

Cited by 48 publications

References 95 publications

Dopaminergic D1 receptor effects on commissural inputs targeting layer V pyramidal subtypes of the mouse medial prefrontal cortex

Dopaminergic D1 receptor effects on commissural inputs targeting layer V pyramidal subtypes of the mouse medial prefrontal cortex

Interpreting in vivo calcium signals from neuronal cell bodies, axons, and dendrites: a review

Ionized calcium in human cerebrospinal fluid and its influence on intrinsic and synaptic excitability of hippocampal pyramidal neurons in the rat

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