Plasticity in prefrontal cortex induced by coordinated nucleus reuniens and hippocampal synaptic transmission

AbstractThe nucleus reuniens of the thalamus (NRe) is reciprocally connected to a range of higher order cortices including hippocampus (HPC) and medial prefrontal cortex (mPFC). The physiological function of NRe is well predicted by requirement for interactions between mPFC and HPC, including associative recognition memory, spatial navigation and working memory. Although anatomical and electrophysiological evidence suggests NRe makes excitatory synapses in mPFC there is little data on the physiological properties of these projections, or whether NRe and HPC target overlapping cell populations and, if so, how they interact. We demonstrate in ex vivo mPFC slices that NRe and HPC afferent inputs converge onto more than two-thirds of layer 5 pyramidal neurons, show that NRe, but not HPC, undergoes marked short-term plasticity at theta, and that HPC, but not NRe, afferents are subject to neuromodulation by acetylcholine acting via muscarinic receptor M2. Finally, we demonstrate that pairing HPC followed by NRe (but not pairing NRe followed by HPC) at theta frequency induces associative, NMDA receptor dependent synaptic plasticity in both inputs to mPFC. These data provide vital physiological phenotypes of the synapses of this circuit and provide a novel mechanism for HPC-NRe-mPFC encoding.

Download Full-text

Plasticity in Prefrontal Cortex Induced by Coordinated Synaptic Transmission Arising from Reuniens/Rhomboid Nuclei and Hippocampus

Cerebral Cortex Communications ◽

10.1093/texcom/tgab029 ◽

2021 ◽

Author(s):

Paul J Banks ◽

E Clea Warburton ◽

Zafar I Bashir

Keyword(s):

Prefrontal Cortex ◽

Pyramidal Neurons ◽

Ex Vivo ◽

Excitatory Synapses ◽

Short Term ◽

Nucleus Reuniens ◽

Short Term Plasticity ◽

Physiological Properties ◽

Theta Frequency ◽

Afferent Inputs

Abstract The nucleus reuniens and rhomboid nuclei of the thalamus (ReRh) are reciprocally connected to a range of higher order cortices including hippocampus (HPC) and medial prefrontal cortex (mPFC). The physiological function of ReRh is well predicted by requirement for interactions between mPFC and HPC, including associative recognition memory, spatial navigation and working memory. Although anatomical and electrophysiological evidence suggests ReRh makes excitatory synapses in mPFC there is little data on the physiological properties of these projections, or whether ReRh and HPC target overlapping cell populations and, if so, how they interact. We demonstrate in ex vivo mPFC slices that ReRh and HPC afferent inputs converge onto more than two-thirds of layer 5 pyramidal neurons, show that ReRh, but not HPC, undergoes marked short-term plasticity during theta frequency transmission, and that HPC, but not ReRh, afferents are subject to neuromodulation by acetylcholine acting via muscarinic receptor M2. Finally, we demonstrate that pairing HPC followed by ReRh (but not pairing ReRh followed by HPC) at theta frequency induces associative, NMDA receptor dependent synaptic plasticity in both inputs to mPFC. These data provide vital physiological phenotypes of the synapses of this circuit and provide a novel mechanism for HPC-ReRh-mPFC encoding.

Download Full-text

Multiple Forms of Short-Term Plasticity at Excitatory Synapses in Rat Medial Prefrontal Cortex

Journal of Neurophysiology ◽

10.1152/jn.2000.83.5.3031 ◽

2000 ◽

Vol 83 (5) ◽

pp. 3031-3041 ◽

Cited By ~ 132

Author(s):

Chris M. Hempel ◽

Kenichi H. Hartman ◽

X.-J. Wang ◽

Gina G. Turrigiano ◽

Sacha B. Nelson

Keyword(s):

Prefrontal Cortex ◽

Medial Prefrontal Cortex ◽

Dynamic Properties ◽

Specific Property ◽

Pyramidal Cells ◽

Excitatory Synapses ◽

Short Term ◽

Short Term Plasticity ◽

Layer V

Short-term synaptic plasticity, in particular short-term depression and facilitation, strongly influences neuronal activity in cerebral cortical circuits. We investigated short-term plasticity at excitatory synapses onto layer V pyramidal cells in the rat medial prefrontal cortex, a region whose synaptic dynamic properties have not been systematically examined. Using intracellular and extracellular recordings of synaptic responses evoked by stimulation in layers II/III in vitro, we found that short-term depression and short-term facilitation are similar to those described previously in other regions of the cortex. In additition, synapses in the prefrontal cortex prominently express augmentation, a longer lasting form of short-term synaptic enhancement. This consists of a 40–60% enhancement of synaptic transmission which lasts seconds to minutes and which can be induced by stimulus trains of moderate duration and frequency. Synapses onto layer III neurons in the primary visual cortex express substantially less augmentation, indicating that this is a synapse-specific property. Intracellular recordings from connected pairs of layer V pyramidal cells in the prefrontal cortex suggest that augmentation is a property of individual synapses that does not require activation of multiple synaptic inputs or neuromodulatory fibers. We propose that synaptic augmentation could function to enhance the ability of a neuronal circuit to sustain persistent activity after a transient stimulus. This idea is explored using a computer simulation of a simplified recurrent cortical network.

Download Full-text

A Simple Depletion Model of the Readily Releasable Pool of Synaptic Vesicles Cannot Account for Paired-Pulse Depression

Journal of Neurophysiology ◽

10.1152/jn.00554.2006 ◽

2007 ◽

Vol 97 (1) ◽

pp. 948-950 ◽

Cited By ~ 10

Author(s):

Jane M. Sullivan

Keyword(s):

Synaptic Vesicles ◽

Hippocampal Neurons ◽

Synaptic Activity ◽

Excitatory Synapses ◽

Short Term ◽

Paired Pulse ◽

Short Term Plasticity ◽

Releasable Pool ◽

Readily Releasable Pool ◽

Paired Pulse Depression

Paired-pulse depression (PPD) is a form of short-term plasticity that plays a central role in processing of synaptic activity and is manifest as a decrease in the size of the response to the second of two closely timed stimuli. Despite mounting evidence to the contrary, PPD is still commonly thought to reflect depletion of the pool of synaptic vesicles available for release in response to the second stimulus. Here it is shown that PPD cannot be accounted for by depletion at excitatory synapses made by hippocampal neurons because PPD is unaffected by changes in the fraction of the readily releasable pool (RRP) released by the first of a pair of pulses.

Download Full-text

A Quantitative Description of Short-Term Plasticity at Excitatory Synapses in Layer 2/3 of Rat Primary Visual Cortex

Journal of Neuroscience ◽

10.1523/jneurosci.17-20-07926.1997 ◽

1997 ◽

Vol 17 (20) ◽

pp. 7926-7940 ◽

Cited By ~ 338

Author(s):

Juan A. Varela ◽

Kamal Sen ◽

Jay Gibson ◽

Joshua Fost ◽

L. F. Abbott ◽

...

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Quantitative Description ◽

Excitatory Synapses ◽

Short Term ◽

Short Term Plasticity ◽

Layer 2

Download Full-text

Distinct forms of short-term plasticity at excitatory synapses of hippocampus and neocortex

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.94.8.4161 ◽

1997 ◽

Vol 94 (8) ◽

pp. 4161-4166 ◽

Cited By ~ 57

Author(s):

M. A. Castro-Alamancos ◽

B. W. Connors

Keyword(s):

Excitatory Synapses ◽

Short Term ◽

Short Term Plasticity

Download Full-text

Demonstration of short-term plasticity in the dorsolateral prefrontal cortex with theta burst stimulation: A TMS-EEG study

Clinical Neurophysiology ◽

10.1016/j.clinph.2017.04.005 ◽

2017 ◽

Vol 128 (7) ◽

pp. 1117-1126 ◽

Cited By ~ 31

Author(s):

Sung Wook Chung ◽

Benjamin P. Lewis ◽

Nigel C. Rogasch ◽

Takashi Saeki ◽

Richard H. Thomson ◽

...

Keyword(s):

Prefrontal Cortex ◽

Dorsolateral Prefrontal Cortex ◽

Theta Burst Stimulation ◽

Burst Stimulation ◽

Short Term ◽

Short Term Plasticity ◽

Dorsolateral Prefrontal ◽

Theta Burst

Download Full-text

Functional Maturation of Excitatory Synapses in Layer 3 Pyramidal Neurons during Postnatal Development of the Primate Prefrontal Cortex

Cerebral Cortex ◽

10.1093/cercor/bhm095 ◽

2007 ◽

Vol 18 (3) ◽

pp. 626-637 ◽

Cited By ~ 54

Author(s):

G. Gonzalez-Burgos ◽

S. Kroener ◽

A. V. Zaitsev ◽

N. V. Povysheva ◽

L. S. Krimer ◽

...

Keyword(s):

Prefrontal Cortex ◽

Postnatal Development ◽

Pyramidal Neurons ◽

Excitatory Synapses ◽

Functional Maturation

Download Full-text

Plasticity in striatal dopamine release is governed by release-independent depression and the dopamine transporter

Nature Communications ◽

10.1038/s41467-019-12264-9 ◽

2019 ◽

Vol 10 (1) ◽

Cited By ~ 6

Author(s):

Mark D. Condon ◽

Nicola J. Platt ◽

Yan-Feng Zhang ◽

Bradley M. Roberts ◽

Michael A. Clements ◽

...

Keyword(s):

Dopamine Transporter ◽

Dopaminergic Neurons ◽

Action Potentials ◽

Dopamine Release ◽

Ex Vivo ◽

Dorsal Striatum ◽

Short Term ◽

Fast Scan Cyclic Voltammetry ◽

Short Term Plasticity ◽

Initial Release

Abstract Mesostriatal dopaminergic neurons possess extensively branched axonal arbours. Whether action potentials are converted to dopamine output in the striatum will be influenced dynamically and critically by axonal properties and mechanisms that are poorly understood. Here, we address the roles for mechanisms governing release probability and axonal activity in determining short‐term plasticity of dopamine release, using fast‐scan cyclic voltammetry in the ex vivo mouse striatum. We show that brief short‐term facilitation and longer short term depression are only weakly dependent on the level of initial release, i.e. are release insensitive. Rather, short-term plasticity is strongly determined by mechanisms which govern axonal activation, including K+‐gated excitability and the dopamine transporter, particularly in the dorsal striatum. We identify the dopamine transporter as a master regulator of dopamine short‐term plasticity, governing the balance between release‐dependent and independent mechanisms that also show region‐specific gating.

Download Full-text

Phosphorylation-State-Dependent Regulation of NMDA Receptor Short-Term Plasticity Modifies Hippocampal Dendritic Ca2+ Transients

Journal of Neurophysiology ◽

10.1152/jn.01081.2009 ◽

2010 ◽

Vol 104 (4) ◽

pp. 2203-2213 ◽

Cited By ~ 4

Author(s):

Debika Chatterjea ◽

Edaeni Hamid ◽

John P. Leonard ◽

Simon Alford

Keyword(s):

Nmda Receptor ◽

Pyramidal Neurons ◽

Long Term Potentiation ◽

Receptor Activation ◽

Short Term ◽

Short Term Plasticity ◽

State Dependent ◽

Term Potentiation ◽

Protocol Enhancement

N-methyl-d-aspartate (NMDA) receptor-mediated currents are enhanced by phosphorylation. We have investigated effects of phosphorylation-dependent short-term plasticity of NMDA receptor-mediated excitatory postsynaptic currents (EPSCs) on the induction of long-term depression (LTD). We confirmed in whole cell clamped CA1 pyramidal neurons that LTD is induced by pairing stimulus protocols. However, after serine-threonine phosphorylation was modified by postsynaptic introduction of a protein phosphatase-1 (PP1) inhibitor, the same pairing protocol evoked long-term potentiation (LTP). We determined effects of modification of phosphatase activity on evoked NMDA EPSCs during LTD induction protocols. During LTD induction, using a protocol pairing depolarization to –40 mV and 0.5 Hz stimulation, NMDA receptor-mediated EPSCs undergo a short-term enhancement at the start of the protocol. In neurons in which PP1 activity was inhibited, this short-term enhancement was markedly amplified. We then investigated the effect of this enhancement on Ca2+ entry during the start of the LTD induction protocol. Enhancement of NMDA receptor-mediated responses was accompanied by an amplification of induction protocol-evoked Ca2+ transients. Furthermore, this amplification required synaptic activation during the protocol, consistent with an enhancement of Ca2+ entry mediated by NMDA receptor activation. The sign of NMDA receptor-mediated long-term plasticity, whether potentiation or depression depends on the amplitude of the synaptic Ca2+ transient during induction. We conclude that short-term phosphorylation-dependent plasticity of the NMDA receptor-mediated EPSCs contributes significantly to the effect of phosphatase inhibition on the subsequent induction of LTD or LTP.

Download Full-text