Nicotine Exposure during Adolescence Leads to Short- and Long-Term Changes in Spike Timing-Dependent Plasticity in Rat Prefrontal Cortex

The induction of long-term potentiation (LTP) and long-term depression (LTD) of excitatory postsynaptic currents was investigated in proximal synapses of layer 2/3 pyramidal cells of the rat medial prefrontal cortex. The spike timing-dependent plasticity (STDP) induction protocol of negative timing, with postsynaptic leading presynaptic stimulation of action potentials (APs), induced LTD as expected from the classical STDP rule. However, the positive STDP protocol of presynaptic leading postsynaptic stimulation of APs predominantly induced a presynaptically expressed LTD rather than the expected postsynaptically expressed LTP. Thus the induction of plasticity in layer 2/3 pyramidal cells does not obey the classical STDP rule for positive timing. This unusual STDP switched to a classical timing rule if the slow Ca2+-dependent, K+-mediated afterhyperpolarization (sAHP) was inhibited by the selective blocker N-trityl-3-pyridinemethanamine (UCL2077), by the β-adrenergic receptor agonist isoproterenol, or by the cholinergic agonist carbachol. Thus we demonstrate that neuromodulators can affect synaptic plasticity by inhibition of the sAHP. These findings shed light on a fundamental question in the field of memory research regarding how environmental and behavioral stimuli influence LTP, thereby contributing to the modulation of memory.

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Dopaminergic Neuromodulation of Spike Timing Dependent Plasticity in Mature Adult Rodent and Human Cortical Neurons

Frontiers in Cellular Neuroscience ◽

10.3389/fncel.2021.668980 ◽

2021 ◽

Vol 15 ◽

Author(s):

Emma Louise Louth ◽

Rasmus Langelund Jørgensen ◽

Anders Rosendal Korshoej ◽

Jens Christian Hedemann Sørensen ◽

Marco Capogna

Keyword(s):

Learning And Memory ◽

Cortical Neurons ◽

Synaptic Depression ◽

Spike Timing ◽

Therapeutic Interventions ◽

Spike Timing Dependent Plasticity ◽

Mature Adult ◽

Dependent Plasticity ◽

Cortical Synapses

Synapses in the cerebral cortex constantly change and this dynamic property regulated by the action of neuromodulators such as dopamine (DA), is essential for reward learning and memory. DA modulates spike-timing-dependent plasticity (STDP), a cellular model of learning and memory, in juvenile rodent cortical neurons. However, it is unknown whether this neuromodulation also occurs at excitatory synapses of cortical neurons in mature adult mice or in humans. Cortical layer V pyramidal neurons were recorded with whole cell patch clamp electrophysiology and an extracellular stimulating electrode was used to induce STDP. DA was either bath-applied or optogenetically released in slices from mice. Classical STDP induction protocols triggered non-hebbian excitatory synaptic depression in the mouse or no plasticity at human cortical synapses. DA reverted long term synaptic depression to baseline in mouse via dopamine 2 type receptors or elicited long term synaptic potentiation in human cortical synapses. Furthermore, when DA was applied during an STDP protocol it depressed presynaptic inhibition in the mouse but not in the human cortex. Thus, DA modulates excitatory synaptic plasticity differently in human vs. mouse cortex. The data strengthens the importance of DA in gating cognition in humans, and may inform on therapeutic interventions to recover brain function from diseases.

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Distributed Network Actions by Nicotine Increase the Threshold for Spike-Timing-Dependent Plasticity in Prefrontal Cortex

Neuron ◽

10.1016/j.neuron.2007.03.006 ◽

2007 ◽

Vol 54 (1) ◽

pp. 73-87 ◽

Cited By ~ 145

Author(s):

Jonathan J. Couey ◽

Rhiannon M. Meredith ◽

Sabine Spijker ◽

Rogier B. Poorthuis ◽

August B. Smit ◽

...

Keyword(s):

Prefrontal Cortex ◽

Spike Timing ◽

Distributed Network ◽

Spike Timing Dependent Plasticity ◽

Dependent Plasticity

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Spike Timing-Dependent Plasticity: From Synapse to Perception

Physiological Reviews ◽

10.1152/physrev.00030.2005 ◽

2006 ◽

Vol 86 (3) ◽

pp. 1033-1048 ◽

Cited By ~ 385

Author(s):

Yang Dan ◽

Mu-Ming Poo

Keyword(s):

Neuronal Excitability ◽

Human Perception ◽

Long Term Potentiation ◽

Spike Timing ◽

Spike Timing Dependent Plasticity ◽

Dependent Plasticity ◽

Functional Changes

Information in the nervous system may be carried by both the rate and timing of neuronal spikes. Recent findings of spike timing-dependent plasticity (STDP) have fueled the interest in the potential roles of spike timing in processing and storage of information in neural circuits. Induction of long-term potentiation (LTP) and long-term depression (LTD) in a variety of in vitro and in vivo systems has been shown to depend on the temporal order of pre- and postsynaptic spiking. Spike timing-dependent modification of neuronal excitability and dendritic integration was also observed. Such STDP at the synaptic and cellular level is likely to play important roles in activity-induced functional changes in neuronal receptive fields and human perception.

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Dopaminergic neuromodulation of spike timing dependent plasticity in mature adult rodent and human cortical neurons

10.1101/2020.05.15.098400 ◽

2020 ◽

Author(s):

Emma Louise Louth ◽

Rasmus Langelund Jørgensen ◽

Anders Rosendal Korshøj ◽

Jens Christian Hedemann Sørensen ◽

Marco Capogna

Keyword(s):

Learning And Memory ◽

Cortical Neurons ◽

Synaptic Depression ◽

Spike Timing ◽

Therapeutic Interventions ◽

Spike Timing Dependent Plasticity ◽

Mature Adult ◽

Dependent Plasticity ◽

Cortical Synapses

AbstractSynapses in the cerebral cortex constantly change and this dynamic property regulated by the action of neuromodulators such as dopamine (DA), is essential for reward learning and memory. DA modulates spike-timing-dependent plasticity (STDP), a cellular model of learning and memory, in juvenile rodent cortical neurons. However, it is unknown whether this neuromodulation also occurs at excitatory synapses of cortical neurons in mature adult mice or in humans. Cortical layer V pyramidal neurons were recorded with whole cell patch clamp electrophysiology and an extracellular stimulating electrode was used to induce STDP. DA was either bath-applied or optogenetically released in slices from mice. Classical STDP induction protocols triggered non-Hebbian excitatory synaptic depression in the mouse or no plasticity at human cortical synapses. DA reverted long term synaptic depression to baseline in mouse or elicited long term synaptic potentiation in human cortical synapses. Furthermore, when DA was applied during a STDP protocol it depressed presynaptic inhibition in the mouse but not in the human cortex. Thus, DA modulates excitatory synaptic plasticity differently in human versus mouse cortex. The data strengthens the importance of DA in gating cognition in humans, and may inform on therapeutic interventions to recover brain function from diseases.

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Long-term population spike-timing-dependent plasticity promotes synaptic tagging but not cross-tagging in rat hippocampal area CA1

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1817643116 ◽

2019 ◽

Vol 116 (12) ◽

pp. 5737-5746 ◽

Cited By ~ 2

Author(s):

Karen Ka Lam Pang ◽

Mahima Sharma ◽

Kumar Krishna-K. ◽

Thomas Behnisch ◽

Sreedharan Sajikumar

Keyword(s):

Synaptic Plasticity ◽

Long Term Potentiation ◽

Neuronal Population ◽

Spike Timing ◽

Spike Timing Dependent Plasticity ◽

Dependent Plasticity ◽

Adult Rat ◽

Term Potentiation ◽

Hippocampal Ca3

In spike-timing-dependent plasticity (STDP), the direction and degree of synaptic modification are determined by the coherence of pre- and postsynaptic activities within a neuron. However, in the adult rat hippocampus, it remains unclear whether STDP-like mechanisms in a neuronal population induce synaptic potentiation of a long duration. Thus, we asked whether the magnitude and maintenance of synaptic plasticity in a population of CA1 neurons differ as a function of the temporal order and interval between pre- and postsynaptic activities. Modulation of the relative timing of Schaffer collateral fibers (presynaptic component) and CA1 axons (postsynaptic component) stimulations resulted in an asymmetric population STDP (pSTDP). The resulting potentiation in response to 20 pairings at 1 Hz was largest in magnitude and most persistent (4 h) when presynaptic activity coincided with or preceded postsynaptic activity. Interestingly, when postsynaptic activation preceded presynaptic stimulation by 20 ms, an immediate increase in field excitatory postsynaptic potentials was observed, but it eventually transformed into a synaptic depression. Furthermore, pSTDP engaged in selective forms of late-associative activity: It facilitated the maintenance of tetanization-induced early long-term potentiation (LTP) in neighboring synapses but not early long-term depression, reflecting possible mechanistic differences with classical tetanization-induced LTP. The data demonstrate that a pairing of pre- and postsynaptic activities in a neuronal population can greatly reduce the required number of synaptic plasticity-evoking events and induce a potentiation of a degree and duration similar to that with repeated tetanization. Thus, pSTDP determines synaptic efficacy in the hippocampal CA3–CA1 circuit and could bias the CA1 neuronal population toward potentiation in future events.

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Faculty Opinions recommendation of Distributed network actions by nicotine increase the threshold for spike-timing-dependent plasticity in prefrontal cortex.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1081865.534797 ◽

2007 ◽

Author(s):

John Dani

Keyword(s):

Prefrontal Cortex ◽

Spike Timing ◽

Distributed Network ◽

Spike Timing Dependent Plasticity ◽

Dependent Plasticity

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Learning complex temporal patterns with resource-dependent spike timing-dependent plasticity

Journal of Neurophysiology ◽

10.1152/jn.01150.2011 ◽

2012 ◽

Vol 108 (2) ◽

pp. 551-566 ◽

Cited By ~ 9

Author(s):

Jason F. Hunzinger ◽

Victor H. Chan ◽

Robert C. Froemke

Keyword(s):

Long Term Potentiation ◽

Spike Timing ◽

Spike Timing Dependent Plasticity ◽

Dependent Plasticity ◽

Rate Dependent ◽

Temporal Relationships ◽

Term Potentiation ◽

Functional Mechanisms

Studies of spike timing-dependent plasticity (STDP) have revealed that long-term changes in the strength of a synapse may be modulated substantially by temporal relationships between multiple presynaptic and postsynaptic spikes. Whereas long-term potentiation (LTP) and long-term depression (LTD) of synaptic strength have been modeled as distinct or separate functional mechanisms, here, we propose a new shared resource model. A functional consequence of our model is fast, stable, and diverse unsupervised learning of temporal multispike patterns with a biologically consistent spiking neural network. Due to interdependencies between LTP and LTD, dendritic delays, and proactive homeostatic aspects of the model, neurons are equipped to learn to decode temporally coded information within spike bursts. Moreover, neurons learn spike timing with few exposures in substantial noise and jitter. Surprisingly, despite having only one parameter, the model also accurately predicts in vitro observations of STDP in more complex multispike trains, as well as rate-dependent effects. We discuss candidate commonalities in natural long-term plasticity mechanisms.

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Interaction between theta-phase and spike-timing dependent plasticity simulates theta induced memory effects

10.1101/2021.11.24.469900 ◽

2021 ◽

Author(s):

Danying Wang ◽

George Michael Parish ◽

Kimron L Shapiro ◽

Simon Hanslmayr

Keyword(s):

Episodic Memory ◽

Theta Rhythm ◽

Long Term Potentiation ◽

Spike Timing ◽

Spike Timing Dependent Plasticity ◽

Cell Culture Study ◽

Dependent Plasticity ◽

Hippocampal Cell Culture ◽

Theta Phase

Rodent studies suggest that spike timing relative to hippocampal theta activity determines whether potentiation or depression of synapses arise. Such changes also depend on spike timing between pre- and post-synaptic neurons, known as spike-timing-dependent plasticity (STDP). STDP, together with theta-phase-dependent learning, has inspired several computational models of learning and memory. However, evidence to elucidate how these mechanisms directly link to human episodic memory is lacking. In a computational model, we modulate long-term potentiation (LTP) and long-term depression (LTD) of STDP, by opposing phases of a simulated theta rhythm. We fit parameters to a hippocampal cell culture study in which LTP and LTD were observed to occur in opposing phases of a theta rhythm. Further, we modulated two inputs by cosine waves with synchronous and asynchronous phase offsets and replicate key findings in human episodic memory. Learning advantage was found for the synchronous condition, as compared to the asynchronous conditions, and was specific to theta modulated inputs. Importantly, simulations with and without each mechanism suggest that both STDP and theta-phase-dependent plasticity are necessary to replicate the findings. Together, the results indicate a role for circuit-level mechanisms, which bridges the gap between slice preparation studies and human memory.

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