Adrenergic modulation of sharp wave‐ripple activity in rat hippocampal slices

Haq, Rizwan ul; Liotta, Agustin; Kovacs, Richard J.; Rösler, Anton; Jarosch, M.J.; Heinemann, Uwe; Behrens, Christoph

doi:10.1002/hipo.20918

Cited by 44 publications

(36 citation statements)

References 52 publications

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“…This in turn will support cAMP-dependent processes underlying LTP and may enable strengthening of weak plasticity. In line with this, it has been reported that β-adrenergic receptor activation enhances CA3 network activity by increasing CA3 burst activity (Jurgens et al, 2005) and facilitates the induction of LTP and sharp-wave ripples (Ul Haq et al, 2011). Under conditions where LTP is induced solely by electrical stimulation of afferent fibers, the LTP that is induced is already “strong.” This induction of very potent and persistent LTP may thus circumvent the need for support through the noradrenergic system and enable cAMP-dependent pathways to be recruited by the stronger activation of glutamatergic receptors or by other neuromodulatory systems.…”

Section: Discussionmentioning

confidence: 63%

Learning-facilitated long-term depression and long-term potentiation at mossy fiber—CA3 synapses requires activation of β-adrenergic receptors

Hagena

Manahan‐Vaughan

2012

Front. Integr. Neurosci.

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Learning-facilitated plasticity refers to hippocampal synaptic plasticity that is facilitated by novel spatial learning events. Both long-term potentiation (LTP) and long-term depression (LTD) are facilitated by novel hippocampus-dependent learning. This has important ramifications for our understanding of how the hippocampus encodes memory. One structure that is rarely studied in vivo, but is believed to be crucially important for working and long-term memory processing is the hippocampal CA3 region. Whereas learning-facilitated plasticity has been described in this structure, the mechanisms underlying this phenomenon have not been explored. The noradrenergic system plays an important role in arousal and qualification of new information as salient. It regulates synaptic plasticity in the dentate gyrus and CA1, but nothing is known about the regulation by the noradrenergic system of synaptic plasticity in the CA3 region. We explored whether β-adrenergic receptors contribute to learning-facilitated plasticity at mossy fiber (mf)-CA3 synapses of behaving rats. We found that receptor antagonism had no effect on basal synaptic transmission, short-term potentiation (STP), short-term depression, LTP, or LTD, that were electrically induced by patterned afferent stimulation. We found, however, that both learning-facilitated LTP and LTD were prevented by antagonism of β-adrenergic receptors, whereas the agonist isoproterenol facilitated STP into LTP. Thus, learning-facilitated and electrically-induced plasticity may not share the same prerequisites. These results support that the mf synapse engages in a distinct aspect of encoding of spatial information that involves both LTP and LTD. Furthermore, changes in arousal that are coupled to new learning are associated with activation of hippocampal β-adrenergic receptors that in turn comprise a key element in this type of information acquisition and processing by the CA3 region.

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Section: Discussionmentioning

confidence: 63%

Learning-facilitated long-term depression and long-term potentiation at mossy fiber—CA3 synapses requires activation of β-adrenergic receptors

Hagena

Manahan‐Vaughan

2012

Front. Integr. Neurosci.

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“…In-vitro recordings were performed in stratum pyramidale of area CA1 and occasionally also in area CA3 using an interface chamber and extracellular glass electrodes (filled with 154 mM NaCl, tip diameter 2-3 μM, resistance 2 to 4 MΩ) as previously reported (Hamon, Stanton, and Heinemann 1987; Ul haq et al 2011). Brief (100 μs) electrical pulses were applied using 25 μm bipolar platinum electrodes (ca.…”

Section: Methodsmentioning

confidence: 99%

“…Evoked signals were obtained using 50 % of the intensity required to induce maximal responses. Two protocols were used for recurrent repetitive stimulation: 10 trains of 10 stimuli each with an inter-train interval of 1 s, or 3 trains of 40 stimuli each with an inter-train interval of 40 s (Wöhrl et al 2007a; Ul haq et al 2011). Stimulation frequencies were between 1 and 100 Hz (to stratum radiatum) or 20 or 200 Hz (stratum lacunosum moleculare).…”

Section: Methodsmentioning

confidence: 99%

Peri-infarct blood–brain barrier dysfunction facilitates induction of spreading depolarization associated with epileptiform discharges

Lapilover

Lippmann

Salar

et al. 2012

Neurobiology of Disease

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Recent studies showed that spreading depolarizations (SDs) occur abundantly in patients following ischemic stroke and experimental evidence suggests that SDs recruit tissue at risk into necrosis. We hypothesized that BBB opening with consequent alterations of the extracellular electrolyte composition and extravasation of albumin facilitates generation of SDs since albumin mediates an astrocyte transcriptional response with consequent disturbance of potassium and glutamate homeostasis. Here we show extravasation of Evans blue-albumin complex into the hippocampus following cortical photothrombotic stroke in the neighbouring neocortex. Using extracellular field potential recordings and exposure to serum electrolytes we observed spontaneous SDs in 80 % of hippocampal slices obtained from rats 24 h after cortical photothrombosis. Hippocampal exposure to albumin for 24 h through intraventricular application together with serum electrolytes lowered the threshold for the induction of SDs in most slices irrespective of the pathway of stimulation. Exposing acute slices from naive animals to albumin led also to a reduced SD threshold. In albumin-exposed slices the onset of SDs was usually associated with larger stimulus-induced accumulation of extracellular potassium, and preceded by epileptiform activity, which was also observed during the recovery phase of SDs. Application of ifenprodil (3μM), an NMDA-receptor type 2 B antagonist, blocked stimulus dependent epileptiform discharges and generation of SDs in slices from animals treated with albumin in-vivo. We suggest that BBB opening facilitates the induction of peri-infarct SDs through impaired homeostasis of K+.

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“…NE was further reported to be involved in facilitation of LTP induction—an effect that is mediated by ß receptors of NE involving also facilitated activation of N-methyl-D-aspartate (NMDA) receptors. Interestingly, ßreceptor agonists of NE facilitated induction not only of LTP but also of SPW-R complexes (Ul Haq et al, 2012). When testing for effects of NE alone, LTP was induced but SPW-R did not appear.…”

Section: Role Of Neuromodulators On Theta Gamma Oscillations Sharp mentioning

confidence: 99%

“…This indicates that during induction of LTP certain synapses increase coupling efficacy but are not yet ready to integrate their activity into a neuronal ensemble. NE blocked stimulation induced SPW-R through activation of alpha-1 receptors for NE (Ul Haq et al, 2012). The underlying mechanism seems to be related to an alteration in presynaptic release probability mediated by effects on transmitter release.…”

Section: Role Of Neuromodulators On Theta Gamma Oscillations Sharp mentioning

confidence: 99%

State-dependencies of learning across brain scales

Ritter

Born

Brecht

et al. 2015

Front. Comput. Neurosci.

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Learning is a complex brain function operating on different time scales, from milliseconds to years, which induces enduring changes in brain dynamics. The brain also undergoes continuous “spontaneous” shifts in states, which, amongst others, are characterized by rhythmic activity of various frequencies. Besides the most obvious distinct modes of waking and sleep, wake-associated brain states comprise modulations of vigilance and attention. Recent findings show that certain brain states, particularly during sleep, are essential for learning and memory consolidation. Oscillatory activity plays a crucial role on several spatial scales, for example in plasticity at a synaptic level or in communication across brain areas. However, the underlying mechanisms and computational rules linking brain states and rhythms to learning, though relevant for our understanding of brain function and therapeutic approaches in brain disease, have not yet been elucidated. Here we review known mechanisms of how brain states mediate and modulate learning by their characteristic rhythmic signatures. To understand the critical interplay between brain states, brain rhythms, and learning processes, a wide range of experimental and theoretical work in animal models and human subjects from the single synapse to the large-scale cortical level needs to be integrated. By discussing results from experiments and theoretical approaches, we illuminate new avenues for utilizing neuronal learning mechanisms in developing tools and therapies, e.g., for stroke patients and to devise memory enhancement strategies for the elderly.

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Adrenergic modulation of sharp wave‐ripple activity in rat hippocampal slices

Cited by 44 publications

References 52 publications

Learning-facilitated long-term depression and long-term potentiation at mossy fiber—CA3 synapses requires activation of β-adrenergic receptors

Learning-facilitated long-term depression and long-term potentiation at mossy fiber—CA3 synapses requires activation of β-adrenergic receptors

Peri-infarct blood–brain barrier dysfunction facilitates induction of spreading depolarization associated with epileptiform discharges

State-dependencies of learning across brain scales

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