Cholinergic modulation of cortical oscillatory dynamics

1995 ◽  
Vol 74 (1) ◽  
pp. 288-297 ◽  
Author(s):  
H. Liljenstrom ◽  
M. E. Hasselmo
Keyword(s):  
Synaptic Transmission ◽  
Time Constant ◽  
Field Potential ◽  
Pyramidal Cells ◽  
Gamma Oscillations ◽  
Theta Oscillations ◽  
Cortical Region ◽  
Cholinergic Modulation ◽  
Neuronal Adaptation ◽  
Oscillatory Dynamics

1. The effect of cholinergic modulation on cortical oscillatory dynamics was studied in a computational model of the piriform (olfactory) cortex. The model included the cholinergic suppression of neuronal adaptation, the cholinergic suppression of intrinsic fiber synaptic transmission, the cholinergic enhancement of interneuron activity, and the cholinergic suppression of inhibitory synaptic transmission. 2. Electroencephalographic (EEG) recordings and field potential recordings from the piriform cortex were modeled with a simplified network in which cortical pyramidal cells were represented by excitatory input/output functions with gain parameters dependent on previous activity. The model incorporated distributed excitatory afferent input and excitatory connections between units. In addition, the model contained two sets of inhibitory units mediating inhibition with different time constants and different reversal potentials. This model can match effectively the patterns of cortical EEG and field potentials, showing oscillatory dynamics in both the gamma (30-80 Hz) and theta (3-10 Hz) frequency range. 3. Cholinergic suppression of neuronal adaptation was modeled by reducing the change in gain associated with previous activity. This caused an increased number of oscillations within the network in response to shock stimulation of the lateral olfactory tract, effectively replicating the effect of carbachol on the field potential response in physiological experiments. 4. Cholinergic suppression of intrinsic excitatory synaptic transmission decreased the prominence of gamma oscillations within the network, allowing theta oscillations to predominate. Coupled with the cholinergic suppression of neuronal adaptation, this caused the network to shift from a nonoscillatory state into an oscillatory state of predominant theta oscillations. This replicates the longer term effect of carbachol in experimental preparations on the EEG potential recorded from the cortex in vivo and from brain-slice preparations of the hippocampus in vitro. Analysis of the model suggests that these oscillations depend upon the time constant of neuronal adaptation rather than the time constant of inhibition or the activity of bursting neurons. 5. Cholinergic modulation may be involved in switching the dynamics of this cortical region between those appropriate for learning and those appropriate for recall. During recall, the spread of activity along intrinsic excitatory connections allows associative memory function, whereas neuronal adaptation prevents the spread of activity between different patterns. During learning, the recall of previously stored patterns is prevented by suppression of intrinsic excitatory connections, whereas the response to the new patterns is enhanced by suppression of neuronal adaptation.

scholarly journals Enhanced Temporal Stability of Cholinergic Hippocampal Gamma Oscillations Following Respiratory Alkalosis In Vitro

2001 ◽  
Vol 85 (5) ◽  
pp. 2063-2069 ◽  
Author(s):  
Kerstin Stenkamp ◽  
J. Matias Palva ◽  
Marylka Uusisaari ◽  
Sebastian Schuchmann ◽  
Dietmar Schmitz ◽  
...  
Keyword(s):  
Time Constant ◽  
Decay Time ◽  
Oscillation Frequency ◽  
Hippocampal Slices ◽  
Temporal Stability ◽  
Field Potential ◽  
Gamma Oscillations ◽  
Decay Time Constant ◽  
The Mean

The decrease in brain CO2 partial pressure (pCO2) that takes place both during voluntary and during pathological hyperventilation is known to induce gross alterations in cortical functions that lead to subjective sensations and altered states of consciousness. The mechanisms that mediate the effects of the decrease in pCO2 at the neuronal network level are largely unexplored. In the present work, the modulation of gamma oscillations by hypocapnia was studied in rat hippocampal slices. Field potential oscillations were induced by the cholinergic agonist carbachol under an N-methyl-D-aspartate (NMDA)-receptor blockade and were recorded in the dendritic layer of the CA3 region with parallel measurements of changes in interstitial and intraneuronal pH (pHo and pHi, respectively). Hypocapnia from 5 to 1% CO2 led to a stable monophasic increase of 0.5 and 0.2 units in pHo and pHi, respectively. The mean oscillation frequency increased slightly but significantly from 32 to 34 Hz and the mean gamma-band amplitude (20 to 80 Hz) decreased by 20%. Hypocapnia induced a dramatic enhancement of the temporal stability of the oscillations, as was indicated by a two-fold increase in the exponential decay time constant fitted to the autocorrelogram. A rise in pHi evoked by the weak base trimethylamine (TriMA) was associated with a slight increase in oscillation frequency (37 to 39 Hz) and a decrease in amplitude (30%). Temporal stability, on the other hand, was decreased by TriMA, which suggests that its enhancement in 1% CO2 was related to the rise in pHo. In 1% CO2, the decay-time constant of the evoked monosynaptic pyramidal inhibitory postsynaptic current (IPSC) was unaltered but its amplitude was enhanced. This increase in IPSC amplitude seems to significantly contribute to the enhancement of temporal stability because the enhancement was almost fully reversed by a low concentration of bicuculline. These results suggest that changes in brain pCO2 can have a strong influence on the temporal modulation of gamma rhythms.

Spike Timing of Lacunosom-Moleculare Targeting Interneurons and CA3 Pyramidal Cells During High-Frequency Network Oscillations In Vitro

2007 ◽  
Vol 98 (1) ◽  
pp. 96-104 ◽  
Author(s):  
Jay Spampanato ◽  
Istvan Mody
Keyword(s):  
High Frequency ◽  
Epileptiform Activity ◽  
Field Potential ◽  
Pyramidal Cells ◽  
Gamma Oscillations ◽  
Spike Timing ◽  
Network Activity ◽  
Network Oscillations ◽  
Ca3 Pyramidal Cells

Network activity in the 200- to 600-Hz range termed high-frequency oscillations (HFOs) has been detected in epileptic tissue from both humans and rodents and may underlie the mechanism of epileptogenesis in experimental rodent models. Slower network oscillations including theta and gamma oscillations as well as ripples are generated by the complex spike timing and interactions between interneurons and pyramidal cells of the hippocampus. We determined the activity of CA3 pyramidal cells, stratum oriens lacunosum-moleculare (O-LM) and s. radiatum lacunosum-moleculare (R-LM) interneurons during HFO in the in vitro low-Mg2+ model of epileptiform activity in GIN mice. In these animals, interneurons can be identified prior to cell-attached recordings by the expression of green-fluorescent protein (GFP). Simultaneous local field potential recordings from s. pyramidale and on-cell recordings of individual interneurons and principal cells revealed three primary firing behaviors of the active cells: 36% of O-LM interneurons and 60% of pyramidal cells fired action potentials at high frequencies during the HFO. R-LM interneurons were biphasic in that they fired at high frequency at the beginning of the HFO but stopped firing before its end. When considering only the highest frequency component of the oscillations most pyramidal cells fired on the rising phase of the oscillation. These data provide evidence for functional distinction during HFOs within otherwise homogeneous groups of O-LM interneurons and pyramidal cells.

scholarly journals Tonic Control of Secretory Acid Sphingomyelinase Over Ventral Hippocampal Synaptic Transmission and Neuron Excitability

2021 ◽  
Vol 15 ◽  
Author(s):  
Chih-Hung Lin ◽  
Johannes Kornhuber ◽  
Fang Zheng ◽  
Christian Alzheimer
Keyword(s):  
Synaptic Transmission ◽  
Synaptic Input ◽  
Antidepressant Drugs ◽  
Field Potential ◽  
Pyramidal Cells ◽  
Acid Sphingomyelinase ◽  
Membrane Hyperpolarization ◽  
Cell Excitability ◽  
Ca1 Pyramidal Cells ◽  
Major Player

The acid sphingomyelinase (ASM) converts sphingomyelin into ceramide. Recent work has advanced the ASM/ceramide system as a major player in the pathogenesis of major depressive disorder (MDD). Indeed, ASM activity is enhanced in MDD patients and antidepressant drugs like fluoxetine act as functional inhibitors of ASM. Here, we employed the specific ASM inhibitor ARC39 to explore the acute effects of the enzyme on hippocampal synaptic transmission and cell excitability in adult mouse brain slice preparations. In both field potential and whole-cell recordings, ARC39 (1–3 μM) enhanced excitatory synaptic input onto ventral hippocampal CA1 pyramidal cells. The specificity of drug action was demonstrated by its lacking effect in slices from ASM knockout mice. In control condition, ARC39 strongly reduced firing in most CA1 pyramidal cells, together with membrane hyperpolarization. Such pronounced inhibitory action of ARC39 on soma excitability was largely reversed when GABAA receptors were blocked. The idea that ARC39 recruits GABAergic inhibition to dampen cell excitability was further reinforced by the drug’s ability to enhance the inhibitory synaptic drive onto pyramidal cells. In pyramidal cells that were pharmacologically isolated from synaptic input, the overall effect of ARC39 on cell firing was inhibitory, but some neurons displayed a biphasic response with a transient increase in firing, suggesting that ARC39 might alter intrinsic firing properties in a cell-specific fashion. Because ARC39 is charged at physiological pH and exerted all its effects within minutes of application, we propose that the neurophysiological actions reported here are due to the inhibition of secretory rather than lysosomal ASM. In summary, the ASM inhibitor ARC39 reveals a tonic control of the enzyme over ventral hippocampal excitability, which involves the intrinsic excitability of CA1 pyramidal cells as well as their excitatory and inhibitory synaptic inputs.

scholarly journals TLR4-activated microglia require IFN-γ to induce severe neuronal dysfunction and death in situ

2015 ◽  
Vol 113 (1) ◽  
pp. 212-217 ◽  
Author(s):  
Ismini E. Papageorgiou ◽  
Andrea Lewen ◽  
Lukas V. Galow ◽  
Tiziana Cesetti ◽  
Jörg Scheffel ◽  
...  
Keyword(s):  
Nitric Oxide ◽  
Field Potential ◽  
Population Expansion ◽  
Pyramidal Cells ◽  
Gamma Oscillations ◽  
Extracellular Potassium ◽  
Neuronal Dysfunction ◽  
No Release ◽  
Ifn Γ

Microglia (tissue-resident macrophages) represent the main cell type of the innate immune system in the CNS; however, the mechanisms that control the activation of microglia are widely unknown. We systematically explored microglial activation and functional microglia–neuron interactions in organotypic hippocampal slice cultures, i.e., postnatal cortical tissue that lacks adaptive immunity. We applied electrophysiological recordings of local field potential and extracellular K+ concentration, immunohistochemistry, design-based stereology, morphometry, Sholl analysis, and biochemical analyses. We show that chronic activation with either bacterial lipopolysaccharide through Toll-like receptor 4 (TLR4) or leukocyte cytokine IFN-γ induces reactive phenotypes in microglia associated with morphological changes, population expansion, CD11b and CD68 up-regulation, and proinflammatory cytokine (IL-1β, TNF-α, IL-6) and nitric oxide (NO) release. Notably, these reactive phenotypes only moderately alter intrinsic neuronal excitability and gamma oscillations (30–100 Hz), which emerge from precise synaptic communication of glutamatergic pyramidal cells and fast-spiking, parvalbumin-positive GABAergic interneurons, in local hippocampal networks. Short-term synaptic plasticity and extracellular potassium homeostasis during neural excitation, also reflecting astrocyte function, are unaffected. In contrast, the coactivation of TLR4 and IFN-γ receptors results in neuronal dysfunction and death, caused mainly by enhanced microglial inducible nitric oxide synthase (iNOS) expression and NO release, because iNOS inhibition is neuroprotective. Thus, activation of TLR4 in microglia in situ requires concomitant IFN-γ receptor signaling from peripheral immune cells, such as T helper type 1 and natural killer cells, to unleash neurotoxicity and inflammation-induced neurodegeneration. Our findings provide crucial mechanistic insight into the complex process of microglia activation, with relevance to several neurologic and psychiatric disorders.

scholarly journals Afferent inputs to cortical fast-spiking interneurons organize pyramidal cell network oscillations at high-gamma frequencies (60–200 Hz)

2014 ◽  
Vol 112 (11) ◽  
pp. 3001-3011 ◽  
Author(s):  
Piotr Suffczynski ◽  
Nathan E. Crone ◽  
Piotr J. Franaszczuk
Keyword(s):  
Local Field ◽  
Local Field Potential ◽  
Field Potential ◽  
Pyramidal Cells ◽  
Gamma Oscillations ◽  
Cortical Activation ◽  
Gamma Activity ◽  
High Gamma ◽  
Fast Spiking ◽  
Gamma Frequencies

High-gamma activity, ranging in frequency between ∼60 Hz and 200 Hz, has been observed in local field potential, electrocorticography, EEG and magnetoencephalography signals during cortical activation, in a variety of functional brain systems. The origin of these signals is yet unknown. Using computational modeling, we show that a cortical network model receiving thalamic input generates high-gamma responses comparable to those observed in local field potential recorded in monkey somatosensory cortex during vibrotactile stimulation. These high-gamma oscillations appear to be mediated mostly by an excited population of inhibitory fast-spiking interneurons firing at high-gamma frequencies and pacing excitatory regular-spiking pyramidal cells, which fire at lower rates but in phase with the population rhythm. The physiological correlates of high-gamma activity, in this model of local cortical circuits, appear to be similar to those proposed for hippocampal ripples generated by subsets of interneurons that regulate the discharge of principal cells.

scholarly journals Theta phase mediates deliberate action switching in human Supplementary Motor Areas

2021 ◽  
Author(s):  
Giovanni Maffei ◽  
Riccardo Zucca ◽  
Jordi Ysard Puigbo ◽  
Diogo Santos Pata ◽  
Marco Galli ◽  
...  
Keyword(s):  
Motor Task ◽  
Gamma Oscillations ◽  
Theta Oscillations ◽  
Motor Sequence ◽  
Action Execution ◽  
Oscillatory Dynamics ◽  
Theta Waves ◽  
Phase Alignment ◽  
Theta Phase ◽  
Motor Areas

The ability to deliberately overwrite ongoing automatic actions is a necessary feature of adaptive behavior. It has been proposed that the supplementary motor areas (SMAs) operate as a controller that orchestrates the switching between automatic and deliberate processes by inhibiting ongoing behaviors and so facilitating the execution of alternative ones. In addition, previous studies support the involvement of SMAs theta waves (4-9 Hz) in cognitive control. However, the exact role of such oscillatory dynamics and their contribution to the control of action are not fully understood. To investigate the mechanisms by which the SMAs support direct control of deliberate behavior, we recorded intracranial electroencephalography (iEEG) activity in humans performing a motor sequence task. Subjects had to perform a "change of plans" motor task requiring habitual movements to be overwritten at unpredictable moments. We found that SMAs were exclusively active during trials that demand action reprogramming in response to the unexpected cue but were silent during automatic action execution. Importantly, SMAs activity was characterized by a distinct temporal pattern, expressed in a stereotypical phase alignment of theta oscillations. More specifically, single trial motor performance was correlated with the trial contribution to the global inter-trial phase coherence, with higher coherence associated with faster trials. In addition, theta phase modulated the amplitude of gamma oscillations, with higher cross-frequency coupling in faster trials. Our results suggest that within frontal cortical networks, theta oscillations could encode a control signal that promotes the execution of deliberate actions.

Flexible Frequency Switching in Adult Mouse Visual Cortex Is Mediated by Competition between Parvalbumin and Somatostatin Expressing Interneurons

2021 ◽  
pp. 1-41
Author(s):  
Justin W. M. Domhof ◽  
Paul H. E. Tiesinga
Keyword(s):  
Visual Cortex ◽  
Network Model ◽  
Visual Stimulation ◽  
Field Potential ◽  
Pyramidal Cells ◽  
Gamma Oscillations ◽  
Neuron Network ◽  
Frequency Bands ◽  
Adult Mice ◽  
Beta Rhythms

Neuronal networks in rodent primary visual cortex (V1) can generate oscillations in different frequency bands depending on the network state and the level of visual stimulation. High-frequency gamma rhythms, for example, dominate the network's spontaneous activity in adult mice but are attenuated upon visual stimulation, during which the network switches to the beta band instead. The spontaneous local field potential (LFP) of juvenile mouse V1, however, mainly contains beta rhythms and presenting a stimulus does not elicit drastic changes in network oscillations. We study, in a spiking neuron network model, the mechanism in adult mice allowing for flexible switches between multiple frequency bands and contrast this to the network structure in juvenile mice that lack this flexibility. The model comprises excitatory pyramidal cells (PCs) and two types of interneurons: the parvalbumin-expressing (PV) and the somatostatinexpressing (SOM) interneuron. In accordance with experimental findings, the pyramidal-PV and pyramidal-SOM cell subnetworks are associated with gamma and beta oscillations, respectively. In our model, they are both generated via a pyramidal-interneuron gamma (PING) mechanism, wherein the PCs drive the oscillations. Furthermore, we demonstrate that large but not small visual stimulation activates SOM cells, which shift the frequency of resting-state gamma oscillations produced by the pyramidal-PV cell subnetwork so that beta rhythms emerge. Finally, we show that this behavior is obtained for only a subset of PV and SOM interneuron projection strengths, indicating that their influence on the PCs should be balanced so that they can compete for oscillatory control of the PCs. In sum, we propose a mechanism by which visual beta rhythms can emerge from spontaneous gamma oscillations in a network model of the mouse V1; for this mechanism to reproduce V1 dynamics in adult mice, balance between the effective strengths of PV and SOM cells is required.

Cellular Mechanisms of Thalamically Evoked Gamma Oscillations in Auditory Cortex

2001 ◽  
Vol 85 (3) ◽  
pp. 1235-1245 ◽  
Author(s):  
William Sukov ◽  
Daniel S. Barth
Keyword(s):  
Auditory Cortex ◽  
Field Potential ◽  
Electrode Array ◽  
Pyramidal Cells ◽  
Gamma Oscillations ◽  
Membrane Properties ◽  
Gamma Activity ◽  
Cellular Mechanisms ◽  
Gamma Frequency ◽  
Fast Oscillations

The purpose of this study was to clarify the neurogenesis of thalamically evoked gamma frequency (∼40 Hz) oscillations in auditory cortex by comparing simultaneously recorded extracellular and intracellular responses elicited with electrical stimulation of the posterior intralaminar nucleus of the thalamus (PIL). The focus of evoked gamma activity was located between primary and secondary auditory cortex using a 64-channel epipial electrode array, and all subsequent intracellular recordings and single-electrode field potential recordings were made at this location. These data indicate that PIL stimulation evokes gamma oscillations in auditory cortex by tonically depolarizing pyramidal cells in the supra- and infragranular layers. No cells revealed endogenous membrane properties capable of producing activity in the gamma frequency band when depolarized individually with injected current, but all displayed both sub- and supra-threshold responses time-locked to extracellular fast oscillations when the population was depolarized by PIL stimulation. We propose that cortical gamma oscillations may be produced and propagated intracortically by network interactions among large groups of neurons when mutually excited by modulatory input from the intralaminar thalamus and that these oscillations do not require specialized pacemaker cells for their neurogenesis.

Modulation of associative memory function in a biophysical simulation of rat piriform cortex

1994 ◽  
Vol 72 (2) ◽  
pp. 659-677 ◽  
Author(s):  
E. Barkai ◽  
R. E. Bergman ◽  
G. Horwitz ◽  
M. E. Hasselmo
Keyword(s):  
Synaptic Transmission ◽  
Associative Memory ◽  
Memory Function ◽  
Piriform Cortex ◽  
Pyramidal Cells ◽  
Afferent Input ◽  
Performance Measure ◽  
Synaptic Connections ◽  
Neuronal Adaptation ◽  
Synaptic Modification

1. Associative memory function was analyzed in a realistic biophysical simulation of rat piriform (olfactory) cortex containing 240 pyramidal cells and 58 each of two types of inhibitory interneurons. Pyramidal cell simulations incorporated six different intrinsic currents and three different synaptic currents. We investigated the hypothesis that acetylcholine sets the appropriate dynamics for learning within the network, whereas removal of cholinergic modulation sets the appropriate dynamics for recall. The associative memory function of the network was tested during recall after simulation of the cholinergic suppression of intrinsic fiber synaptic transmission and the cholinergic suppression of neuronal adaptation during learning. 2. Hebbian modification of excitatory synaptic connections between pyramidal cells during learning of patterns of afferent activity allowed the model to show the basic associative memory property of completion during recall in response to degraded versions of those patterns, as evaluated by a performance measure based on normalized dot products. 3. During learning of multiple overlapping patterns of afferent activity, recall of previously learned patterns interfered with the learning of new patterns. As more patterns were stored this interference could lead to the exponential growth of a large number of excitatory synaptic connections within the network. This runaway synaptic modification during learning led to excessive excitatory activity during recall, preventing the accurate recall of individual patterns. 4. Runaway synaptic modification of excitatory intrinsic connections could be prevented by selective suppression of synaptic transmission at these synapses during learning. This allowed effective recall of single learned afferent patterns in response to degraded versions of those patterns, without interference from other learned patterns. 5. During learning, cholinergic suppression of neuronal adaptation enhanced the activity of cortical pyramidal cells in response to afferent input, compensating for decreased activity due to suppression of intrinsic fiber synaptic transmission. This modulation of adaptation led to more rapid learning of afferent input patterns, as demonstrated by higher values of the performance measure. 6. During recall, when suppression of excitatory intrinsic synaptic transmission was removed, continued cholinergic suppression of neuronal adaptation led to the spread of excessive activity. More stable activity patterns during recall could be obtained when the cholinergic suppression of neuronal adaptation was removed at the same time as the cholinergic suppression of synaptic transmission. 7. A realistic biophysical simulation of the effects of acetylcholine on synaptic transmission and neuronal adaptation in the piriform cortex shows that these effects act together to set the appropriate dynamics for learning, whereas removal of both effects sets the appropriate dynamics for recall.

scholarly journals Analog closed-loop optogenetic modulation of hippocampal pyramidal cells dissociates gamma frequency and amplitude

2018 ◽  
Author(s):  
Elizabeth Nicholson ◽  
Dmitry A Kuzmin ◽  
Marco Leite ◽  
Thomas E Akam ◽  
Dimitri M Kullmann
Keyword(s):  
Closed Loop ◽  
Sensory Information ◽  
Pyramidal Cells ◽  
Gamma Oscillations ◽  
Average Frequency ◽  
Oscillatory Dynamics ◽  
Gamma Frequency ◽  
Rate Coding ◽  
And Performance ◽  
Frequency Of Action Potentials

AbstractGamma-band oscillations are implicated in modulation of attention and integration of sensory information. The finding that cross-regional coherence varies with task and performance suggests a role for gamma oscillations in flexible communication among anatomically connected brain areas. How networks become entrained is incompletely understood. Specifically, it is unclear how the spectral and temporal characteristics of network oscillations can be altered on rapid timescales needed for efficient communication. We use closed-loop optogenetic modulation of principal cell excitability to interrogate the dynamical properties of hippocampal oscillations. Gamma frequency and amplitude can be modulated bi-directionally, and dissociated, by phase-advancing or delaying optogenetic feedback to pyramidal cells. Closed-loop modulation alters the synchrony rather than average frequency of action potentials, in principle avoiding disruption of population rate-coding of information. Modulation of phasic excitatory currents in principal neurons is sufficient to manipulate oscillations, suggesting that feed-forward excitation of pyramidal cells has an important role in determining oscillatory dynamics and the ability of networks to couple with one another.

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