Network state-dependent inhibition of identified hippocampal CA3 axo-axonic cells in vivo

Viney, Tim J.; Lasztóczi, Bálint; Katona, Linda; Crump, Michael; Tukker, John J.; Klausberger, Thomas; Somogyi, Péter

doi:10.1038/nn.3550

Cited by 144 publications

(226 citation statements)

References 51 publications

(105 reference statements)

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“…In support of this hypothesis, adding the muscarinergic drug carbachol to the perfusion solution in in vitro investigation also abolishes spontaneously occurring SPW-Rs (16). Alternatively, or in addition, suppression of hippocampal axo-axonic neurons by transiently bursting septal GABAergic neurons may initiate SPW-Rs (40). This suggestion, however, leaves open the question of why a specific subset of septal inhibitory cells bursts during reduced cholinergic activity in the absence of theta oscillation.…”

Section: Discussionmentioning

confidence: 89%

Optogenetic activation of septal cholinergic neurons suppresses sharp wave ripples and enhances theta oscillations in the hippocampus

Vandecasteele

Varga

Berényi

et al. 2014

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

333

317

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Theta oscillations in the limbic system depend on the integrity of the medial septum. The different populations of medial septal neurons (cholinergic and GABAergic) are assumed to affect different aspects of theta oscillations. Using optogenetic stimulation of cholinergic neurons in ChAT-Cre mice, we investigated their effects on hippocampal local field potentials in both anesthetized and behaving mice. Cholinergic stimulation completely blocked sharp wave ripples and strongly suppressed the power of both slow oscillations (0.5-2 Hz in anesthetized, 0.5-4 Hz in behaving animals) and supratheta (6-10 Hz in anesthetized, 10-25 Hz in behaving animals) bands. The same stimulation robustly increased both the power and coherence of theta oscillations (2-6 Hz) in urethane-anesthetized mice. In behaving mice, cholinergic stimulation was less effective in the theta (4-10 Hz) band yet it also increased the ratio of theta/slow oscillation and theta coherence. The effects on gamma oscillations largely mirrored those of theta. These findings show that medial septal cholinergic activation can both enhance theta rhythm and suppress peri-theta frequency bands, allowing theta oscillations to dominate.S ubcortical neuromodulators play a critical role in shifting states of the brain (1, 2). State changes can occur both during sleep and in the waking animal and are instrumental in affecting local circuit computation that supports various functions, including attention, learning, memory, and action (3-5). The septo-hippocampal cholinergic system has been hypothesized to play a critical role in setting network states in the limbic system (4, 6). ACh can affect both short-and long-term plasticity of synaptic connections and provide favorable conditions for encoding information (7-9). These plastic states are associated with hippocampal theta oscillations (10). High theta states are characterized by increased release of ACh that varies in a task-dependent manner on the time scale of seconds (11-13). In contrast, reduced cholinergic activity allows effective spread of excitation in the recurrent CA3 network, giving rise to synchronous sharp wave ripples (SPW-R) (14-16).Inactivation of the medial septum (MS)/diagonal band of Broca abolishes theta oscillations in the hippocampus and entorhinal cortex (17) and results in severe learning deficit (18,19). Similarly, selective toxin lesion of septal cholinergic neurons produces a several-fold decrease of theta power but not its frequency (20). The phase of the local field potentials (LFP) theta oscillations shifts from the septal to the temporal pole and in the CA3-CA1 axis by ∼180° (21, 22). Thus, at each point in time neurons residing at different locations of the three-dimensional structure of the hippocampus spike at different theta phases yet are bound together by the global theta signal. These numerous sources of theta generators are believed to be coordinated by the reciprocal connections between the septum and hippocampus (23), but the nature of this spatial-temporal coordination is n...

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Section: Discussionmentioning

confidence: 89%

Optogenetic activation of septal cholinergic neurons suppresses sharp wave ripples and enhances theta oscillations in the hippocampus

Vandecasteele

Varga

Berényi

et al. 2014

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

333

317

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“…88 Moreover, axo-axonic cells in the CA3 network show significant phase coupling to hippocampal gamma oscillations in vivo, comparable in strength and phase to those of pyramidal cells and PV þ basket cells. 91 In the rat somatosensory cortex, axoaxonic cells have been reported to depolarize pyramidal cells and thus initiate stereotyped series of synaptic events in neuronal networks because of a depolarized reversal potential for axonal relative to perisomatic GABAergic inputs. 92 Further studies are required to clarify the crucial role of axo-axonic cells as suggested by their morphology and strategical positioning.…”

Section: Hippocampal Gamma Oscillations and Fast-spiking Inhibitory Imentioning

confidence: 99%

Highly Energized Inhibitory Interneurons are a Central Element for Information Processing in Cortical Networks

Kann

Papageorgiou

Draguhn

2014

J Cereb Blood Flow Metab

236

235

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Gamma oscillations (B30 to 100 Hz) provide a fundamental mechanism of information processing during sensory perception, motor behavior, and memory formation by coordination of neuronal activity in networks of the hippocampus and neocortex. We review the cellular mechanisms of gamma oscillations about the underlying neuroenergetics, i.e., high oxygen consumption rate and exquisite sensitivity to metabolic stress during hypoxia or poisoning of mitochondrial oxidative phosphorylation. Gamma oscillations emerge from the precise synaptic interactions of excitatory pyramidal cells and inhibitory GABAergic interneurons. In particular, specialized interneurons such as parvalbumin-positive basket cells generate action potentials at high frequency ('fast-spiking') and synchronize the activity of numerous pyramidal cells by rhythmic inhibition ('clockwork'). As prerequisites, fast-spiking interneurons have unique electrophysiological properties and particularly high energy utilization, which is reflected in the ultrastructure by enrichment with mitochondria and cytochrome c oxidase, most likely needed for extensive membrane ion transport and g-aminobutyric acid metabolism. This supports the hypothesis that highly energized fast-spiking interneurons are a central element for cortical information processing and may be critical for cognitive decline when energy supply becomes limited ('interneuron energy hypothesis'). As a clinical perspective, we discuss the functional consequences of metabolic and oxidative stress in fast-spiking interneurons in aging, ischemia, Alzheimer's disease, and schizophrenia.

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“…To examine whether sEPSC supra reinforcement is driven by reward stimulation or by contingency of electrical stimulation of the brain, we applied contingent electrical stimulation to the ventromedial thalamus, a reward-unrelated thalamic nucleus that is located close to the LH and projects to the hippocampus (Su and Bentivoglio, 1990;Varela et al, 2013). Stimulation to the ventromedial thalamus was not shown to increase the sEPSC supra frequency, at least during our 25 min observation period ( p ϭ 0.11, t 4 ϭ 2.04, paired t test, n ϭ 5 cells; Fig.…”

Section: Reinforcement Of Synaptic Activitymentioning

confidence: 99%

“…Cell assembly dynamics have been well documented in coordinated activity of the hippocampus (Harris et al, 2003;, a brain region involved in certain forms of learning and memory. For example, cell assemblies that appeared during learning are often spontaneously reactivated as synchronous barrages during quiet awake states or slow-wave sleep (Buzsáki et al, 1983;Wilson and McNaughton, 1994;Lee and Wilson, 2002). Therefore, barrage activities of hippocampal neurons serve as an experimental model with which to investigate neural processes underlying learning and memory.…”

Section: Introductionmentioning

confidence: 99%

“…However, no studies have addressed the synaptic dynamics that mediates the control of a single neuron's firing. Moreover, in these pioneer studies, the activity of the controlled neuron might be correlated with some feature in the real world, including behavior, cognition, attention, and extrinsic rewards such as food or money (Basmajian, 1963;Fetz, 1969;Fetz and Finocchio, 1975;Fetz, 2007;Cerf et al, 2010;Kobayashi et al, 2010;Schafer and Moore, 2011;Sakurai and Takahashi, 2013).…”

Section: Introductionmentioning

confidence: 99%

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Operant Conditioning of Synaptic and Spiking Activity Patterns in Single Hippocampal Neurons

et al. 2014

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Learning is a process of plastic adaptation through which a neural circuit generates a more preferable outcome; however, at a microscopic level, little is known about how synaptic activity is patterned into a desired configuration. Here, we report that animals can generate a specific form of synaptic activity in a given neuron in the hippocampus. In awake, head-restricted mice, we applied electrical stimulation to the lateral hypothalamus, a reward-associated brain region, when whole-cell patch-clamped CA1 neurons exhibited spontaneous synaptic activity that met preset criteria. Within 15 min, the mice learned to generate frequently the excitatory synaptic input pattern that satisfied the criteria. This reinforcement learning of synaptic activity was not observed for inhibitory input patterns. When a burst unit activity pattern was conditioned in paired and nonpaired paradigms, the frequency of burst-spiking events increased and decreased, respectively. The burst reinforcement occurred in the conditioned neuron but not in other adjacent neurons; however, ripple field oscillations were concomitantly reinforced. Neural conditioning depended on activation of NMDA receptors and dopamine D 1 receptors. Acutely stressed mice and depression model mice that were subjected to forced swimming failed to exhibit the neural conditioning. This learning deficit was rescued by repetitive treatment with fluoxetine, an antidepressant. Therefore, internally motivated animals are capable of routing an ongoing action potential series into a specific neural pathway of the hippocampal network.

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Network state-dependent inhibition of identified hippocampal CA3 axo-axonic cells in vivo

Cited by 144 publications

References 51 publications

Optogenetic activation of septal cholinergic neurons suppresses sharp wave ripples and enhances theta oscillations in the hippocampus

Optogenetic activation of septal cholinergic neurons suppresses sharp wave ripples and enhances theta oscillations in the hippocampus

Highly Energized Inhibitory Interneurons are a Central Element for Information Processing in Cortical Networks

Operant Conditioning of Synaptic and Spiking Activity Patterns in Single Hippocampal Neurons

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