Central core modulation of spontaneous oscillations and sensory transmission in thalamocortical systems

doi:10.1016/0959-4388(93)90064-6

Current Opinion in Neurobiology

Volume 3, Issue 4, August 1993, Pages 619-625

https://doi.org/10.1016/0959-4388(93)90064-6 Get rights and content

Abstract

Central core (brainstem, diencephalic and basal forebrain) systems influence the functional modes of thalamic and cortical neurons during behavioral states of vigilance. Recent studies in vivo and in vitro have focused on the cellular properties of central core systems and their modulation of slow sleep oscillations, fast rhythms during arousal and dreaming state, and the fine inhibitory sculpturing of afferent signals.

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During NREM/slow wave sleep, cortical UP-DOWN states of alternating depolarization and hyperpolarization are observed that are associated with the generation of slow delta waves (∼1–4 Hz) and faster spindles (∼11–16 Hz) (Steriade and Timofeev, 2003; Fuentealba et al., 2004). Sleep spindles are generated by the interaction between the GABAergic neurons of the thalamic reticular nucleus and the thalamocortical nuclei, and are coupled to the cortical delta waves (Steriade, 1993c, b, a; Steriade et al., 1993c; Steriade et al., 1993b, a; Fernandez and Luthi, 2020). There is emerging evidence for a hippocampal-neocortical dialogue during NREM sleep through SPW-Rs, delta waves, and spindles, and for their role in learning, memory consolidation and interregional transfer of information (Buzsaki, 1996; Buzsaki and Peyrache, 2013; Buzsaki, 2015; Maingret et al., 2016; Seibt et al., 2016; Antony et al., 2019; Kim et al., 2019; Todorova and Zugaro, 2019; Karimi Abadchi et al., 2020; Peyrache and Seibt, 2020; Dickey et al., 2021).
Neurons and glial cells are endowed with membranes that express a rich repertoire of ion channels, transporters, and receptors. The constant flux of ions across the neuronal and glial membranes results in voltage fluctuations that can be recorded from the extracellular matrix. The high frequency components of this voltage signal contain information about the spiking activity, reflecting the output from the neurons surrounding the recording location. The low frequency components of the signal, referred to as the local field potential (LFP), have been traditionally thought to provide information about the synaptic inputs that impinge on the large dendritic trees of various neurons. In this review, we discuss recent computational and experimental studies pointing to a critical role of several active dendritic mechanisms that can influence the genesis and the location-dependent spectro-temporal dynamics of LFPs, spanning different brain regions. We strongly emphasize the need to account for the several fast and slow dendritic events and associated active mechanisms — including gradients in their expression profiles, inter- and intra-cellular spatio-temporal interactions spanning neurons and glia, heterogeneities and degeneracy across scales, neuromodulatory influences, and activitydependent plasticity — towards gaining important insights about the origins of LFP under different behavioral states in health and disease. We provide simple but essential guidelines on how to model LFPs taking into account these dendritic mechanisms, with detailed methodology on how to account for various heterogeneities and electrophysiological properties of neurons and synapses while studying LFPs.
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The post stimulation beta ERS has been suggested to serve as a selective deactivation process or “active inhibition” in the somatosensory cortex (Neuper and Pfurtscheller, 2001). Beta band activity has also been linked to enhanced alertness in thalamo-cortical systems, such that augmented beta oscillations suggest an activation of the somatosensory or motor cortex by motor preparation or focused attention (Steriade, 1993). Further evidence for attention related beta oscillations comes from the correlation of augmented sensorimotor beta power with attention focused on a motor event (Muthukumaraswamy and Singh, 2008) and an improvement in sensorimotor performance (Egner and Gruzelier, 2004; Vernon et al., 2003).
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These results further corroborate the involvement of the subthalamic nucleus in somatosensory processing.
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Loss of righting reflex (LORR) occurred with 5.63 ng ml⁻¹. Dexmedetomidine produced a linear concentration-dependent attenuation of cortical (P<0.04) and thalamic (P ≤ 0.0051) log power in all bands. Slopes for cortex and thalamus were similar. The slope for dexmedetomidine on thalamic power in the 76–200 Hz range was less than half that of the other agents (P<0.003). LORR was associated with an increase in delta band (0.3–4.0 Hz) thalamocortical coherence (P<0.001). Increased low-frequency coherence also occurred with propofol and isoflurane.
Dexmedetomidine attenuates high-frequency thalamocortical rhythms, but to a lesser degree than isoflurane and propofol. The main differences between dexmedetomidine and the other anaesthetics involved thalamic rhythms, further substantiating the link between impaired thalamic function and anaesthesia. Increased delta coherence likely reflects cyclic hyperpolarization of thalamocortical networks and may be a marker for loss of consciousness.
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The laterodorsal tegmental nucleus (LDTg) and the pedunculopontine tegmental nucleus (PPTg) provide cholinergic inputs to the thalamus, including the ILN, and to the cortex (e.g., Berendse and Groenewegen, 1991; Hallanger and Wainer, 1988; Herkenham, 1980; Rye et al., 1987;; rev Jones, 2004, Fig. 3B). The LDTg and PPTg are implicated in the switch from SWS to REM sleep or to wakefulness states by blocking spindle generation (e.g., Steriade, 1993; Steriade et al., 1990). Recent data showed that cells in the ARAS, particularly the PPTg neurons, exhibit both electrical coupling, mainly GABAergic, and gamma band activity, providing a new mechanism for sleep-wake control and consciousness maintenance (rev Urbano et al., 2012).
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Although electrophysiological techniques offer a good alternative, our understanding of the relationship between pain and network connectivity in the brain at the electrophysiological level is biased toward single-unit physiology under anesthesia, compared to multi-unit or population coding in the awake state [52]. Thalamocortical connections generate rhythmic activity referred to as oscillations, which are critical for the processing of sensory information [62]. Expectedly, painful sensory experiences modulate thalamocortical oscillations (oscillatory rhythms generated by reciprocal thalamocortical connections); however, the directionality of such modulation remains unresolved.
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In the central nervous system, anesthetics target specific receptors that are drug-dependent [1]. A reasonable understanding of the pharmacological effects of anesthetics exists today [2], but very little is known regarding the neural mechanisms by which this receptor binding results in sedation and loss of consciousness. General anesthesia (GA) could be defined as a reversible drug-induced state leading to unconsciousness, amnesia, analgesia and immobility along with physiological stability [3].
How does general anesthesia (GA) work? Anesthetics are pharmacological agents that target specific central nervous system receptors. Once they bind to their brain receptors, anesthetics modulate remote brain areas and end up interfering with global neuronal networks, leading to a controlled and reversible loss of consciousness. This remarkable manipulation of consciousness allows millions of people every year to undergo surgery safely most of the time. However, despite all the progress that has been made, we still lack a clear and comprehensive insight into the specific neurophysiological mechanisms of GA, from the molecular level to the global brain propagation. During the last decade, the exponential progress in neuroscience and neuro-imaging led to a significant step in the understanding of the neural correlates of consciousness, with direct consequences for clinical anesthesia. Far from shutting down all brain activity, anesthetics lead to a shift in the brain state to a distinct, highly specific and complex state, which is being increasingly characterized by modern neuro-imaging techniques. There are several clinical consequences and challenges that are arising from the current efforts to dissect GA mechanisms: the improvement of anesthetic depth monitoring, the characterization and avoidance of intra-operative awareness and post-anesthesia cognitive disorders, and the development of future generations of anesthetics.
Comment marche l’anesthésie générale (AG)? Les agents anesthésiques sont des molécules pharmacologiques qui ciblent des récepteurs spécifiques du système nerveux central. Une fois liés à leurs récepteurs cérébraux, ils modulent des régions cérébrales diffuses interférant avec les réseaux neuronaux et conduisent à une perte de conscience contrôlée et réversible. Cette manipulation remarquable de la conscience permet chaque année à des millions de personnes d’avoir une intervention chirurgicale en toute sécurité la plupart du temps. Cependant, malgré tous les progrès accomplis, il nous manque encore une vision claire et exhaustive des mécanismes neurophysiologiques spécifiques de l’AG, du niveau moléculaire jusqu’au niveau global cérébral. Au cours de la dernière décennie, les progrès exponentiels en neurosciences et en neuro-imagerie ont conduit à une étape importante dans la compréhension des corrélats neuronaux de la conscience, avec des conséquences directe pour l’anesthésie clinique. Loin d’arrêter l’activité cérébrale complètement, les agents anesthésiques conduisent à un changement de l’état du cerveau, distinct, très spécifique et complexe, qui est de plus en plus caractérisé par des techniques de neuro-imagerie moderne. Il y a plusieurs conséquences cliniques et de nombreux défis qui se découlent des efforts actuels visant à disséquer les mécanismes de l’AG : l’amélioration de la surveillance de la profondeur de l’anesthésie, la caractérisation et l’évitement du phénomène de mémorisation et des troubles cognitifs post-anesthésie, le développement des futures générations d’agents anesthésiques.

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Central core modulation of spontaneous oscillations and sensory transmission in thalamocortical systems

Abstract

Neuroscience

Neuroscience

J Neurophysiol

J Physiol (Lond)

J Physiol (Lond)

Neuroscience

J Neurosci

J Physiol (Lond)

Neuron

Neuroscience

J Comp Neurol

J Neurosci

J Neurophysiol

Alertness, Quiet Sleep, Dreaming

Brainstem Control of Wakefulness and Sleep

Membrane Properties of Mesopontine Cholinergic Neurons Studied with the Whole-Cell Patch-Clamp Technique: Implications for Behavioral State Control

J Neurophysiol

Serotonin Hyperpolarizes Cholinergic Low-Threshold Burst Neurons in the Rat Laterodorsal Tegmental Neurons In Vitro

Serotonin1 and Serotonin2 Receptors Hyperpolarize and Depolarize Separate Populations of Medial Pontine Reticular Formation Neurons In Vitro

Neuroscience

Excitatory Amino Acids-Mediated Responses and Synaptic Potentials in Medial Reticular Formation Neurons of the Rat In Vitro

J Neurosci

Cellular Substrates of Brain Rhythms

Potentiation of Electroencephalographic Spindles by Ibotenic Microinjections into Nucleus Reticularis Thalami of Cats

Neuroscience

A Novel T-Type Current Underlies Prolonged Ca2+-Dependent Burst Firing in GABAergic Neurons of Rat Thalamic Reticular Nucleus

J Neurosci

Contralateral Pallidothalamic and Pallidotegmental Projections in Primates: and Anterograde and Retrograde Labeling Study

Brain Res

Crosstalk Between the Two Sides of the Thalamus Through the Reticular Nucleus: a Retrograde and Anterograde Tracing Study in the Rat

J Comp Neurol

The Reticular Thalamic Nucleus Projects to the Contralateral Dorsal Thalamus in Macaque Monkey

Neurosci Lett

Involvement of Intrathalamic GABAB Neurotransmission in the Control of Absence Seizures in the Rat

Neuroscience

Properties of a Hyperpolarization-Activated Cation Current and its Role in Rhythmic Oscillation in Thalamic Relay Neurones

J Physiol (Lond)

Electrophysiology of a Slow (0.5–4 Hz) Intrinsic Oscillation of Cat Thalamocortical Neurones In Vivo

J Physiol (Lond)

Serotonin₁ and Serotonin₂ Receptors Hyperpolarize and Depolarize Separate Populations of Medial Pontine Reticular Formation Neurons In Vitro

A Novel T-Type Current Underlies Prolonged Ca²⁺-Dependent Burst Firing in GABAergic Neurons of Rat Thalamic Reticular Nucleus

Involvement of Intrathalamic GABA_B Neurotransmission in the Control of Absence Seizures in the Rat