Article

Delta frequency (1-4 Hz) oscillations of perigeniculate thalamic neurons and their modulation by light.

Laboratoire de Neurophysiologie, Faculté de Médecine, Université Laval, Quebec, Canada.
Neuroscience (impact factor: 3.38). 12/1992; 51(2):285-94. pp.285-94
Source: PubMed

ABSTRACT Neurons in the perigeniculate sector of the reticular thalamic nuclear complex were recorded extra- and intracellularly under deep urethane anesthesia. They were identified by burst responses to optic chiasm stimulation and depolarizing spindle oscillations in response to internal capsule stimulation. Perigeniculate neurons displayed oscillations within the frequency range of electroencephalogram delta waves (1-4 Hz). One-third of extracellularly recorded neurons discharged rhythmic (2.5-4 Hz), high-frequency (150-200 Hz) spike bursts. This was similar to an intrinsic oscillation that was recently observed in dorsal lateral geniculate cells studied in vitro and in vivo. Other oscillating neurons displayed trains of single spikes (20-50 Hz) crowning rhythmic (2.5-4 Hz) depolarizing envelopes that were best expressed at the "resting" membrane potential (-60 to -65 mV). It is suggested that this oscillation reflects synaptic drives from dorsal lateral geniculate neurons. Changes in ambient room luminosity disrupted both types of delta rhythms. These data demonstrate for the first time that delta oscillations are present in the visual sector of the reticular thalamic nucleus. The results suggest that the two types of delta rhythmicity result from intrinsic and network properties of visual thalamic neurons and that perigeniculate cells may synchronize, through backward connections, the activity of dorsal lateral geniculate cells during deep stages of resting sleep.

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    Article: T-type Ca 2+ channels, SK2 channels and SERCAs gate sleep-related oscillations in thalamic dendrites
    Lucius Cueni, Marco Canepari, Rafael Luján, Yann Emmenegger, Masahiko Watanabe, Chris T Bond, Paul Franken, John P Adelman, Anita Lüthi
    [show abstract] [hide abstract]
    ABSTRACT: T-type Ca 21 channels (T channels) underlie rhythmic burst discharges during neuronal oscillations that are typical during sleep. However, the Ca 21 -dependent effectors that are selectively regulated by T currents remain unknown. We found that, in dendrites of nucleus reticularis thalami (nRt), intracellular Ca 21 concentration increases were dominated by Ca 21 influx through T channels and shaped rhythmic bursting via competition between Ca 21 -dependent small-conductance (SK)-type K 1 channels and Ca 21 uptake pumps. Oscillatory bursting was initiated via selective activation of dendritically located SK2 channels, whereas Ca 21 sequestration by sarco/endoplasmic reticulum Ca 21 -ATPases (SERCAs) and cumulative T channel inactivation dampened oscillations. Sk2 –/– (also known as Kcnn2) mice lacked cellular oscillations, showed a greater than threefold reduction in low-frequency rhythms in the electroencephalogram of non–rapid-eye-movement sleep and had disrupted sleep. Thus, the interplay of T channels, SK2 channels and SERCAs in nRt dendrites comprises a specialized Ca 21 signaling triad to regulate oscillatory dynamics related to sleep. Neurons in the thalamocortical system cooperate to produce synchro-nized, rhythmic network activity, which underlies the slow waves that are characteristic of sleep electroencephalograms (EEGs) 1,2 . Rhythmo-genesis is accompanied by low-threshold burst discharges in thalamic neurons 2,3 , which are carried by the three members of the low voltage– activated Ca v 3 Ca 2+ channel family, also called T channels 4 . Although Ca 2+ ions entering through T channels are the electrical charge carriers underlying low-threshold bursts, the associated intracellular Ca 2+ concentration ([Ca 2+ ] i) dynamics, the intracellular Ca 2+ signaling and their role in sleep physiology remain largely unknown. To investigate Ca 2+ -dependent mechanisms that govern oscillatory rhythms important for sleep, we focused on the nRt, a thin inhibitory network interposed between thalamocortical projection neurons and the cortex that is crucial for information transfer and arousal control 5,6 . Prominent forms of rhythmic bursting in the nRt accompany the major types of low-frequency EEG oscillations: in particular, delta oscillations (1–4 Hz), spindle waves (10–15 Hz) and slow oscillations (o1 Hz), with low-threshold bursts showing peculiarly long durations and high numbers of superimposed action potentials 1,2,5–7 . T channels in nRt are composed of Ca v 3.2 and Ca v 3.3 subunits 8 , and are heavily expressed along the somatodendritic axis 9 . In nRt neurons, bursts are typically followed by an afterhyperpolarization (AHP) generated by small-conductance Ca 2+ -activated SK-type K + currents 10–12 . The dynamics and synchrony of these endogenous oscillatory activities are shaped by corticothalamic and thalamocortical excitatory input and by reciprocal connections between nRt cells 1,13 . Here we report a highly specialized Ca 2+ signaling network in nRt dendrites, in which Ca 2+ influx through T channels has a dominant role. Ca 2+ influx activates competing targets, SK2 channels and SERCAs to generate and regulate the strength of nRt oscillations. In Sk2 –/– mice, non–rapid-eye-movement sleep (NREMS) EEG power density was markedly reduced in the delta and spindle frequencies, and sleep was fragmented. Our findings suggest that Ca 2+ influx through T channels acts in concert with SK2 channels and SERCAs to influence characteristic frequency bands of NREMS.
  • Source
    Article: T-type Ca2+ channels, SK2 channels and SERCAs gate sleep-related oscillations in thalamic dendrites.
    Lucius Cueni, Marco Canepari, Rafael Luján, Yann Emmenegger, Masahiko Watanabe, Chris T Bond, Paul Franken, John P Adelman, Anita Lüthi
    [show abstract] [hide abstract]
    ABSTRACT: T-type Ca2+ channels (T channels) underlie rhythmic burst discharges during neuronal oscillations that are typical during sleep. However, the Ca2+-dependent effectors that are selectively regulated by T currents remain unknown. We found that, in dendrites of nucleus reticularis thalami (nRt), intracellular Ca2+ concentration increases were dominated by Ca2+ influx through T channels and shaped rhythmic bursting via competition between Ca2+-dependent small-conductance (SK)-type K+ channels and Ca2+ uptake pumps. Oscillatory bursting was initiated via selective activation of dendritically located SK2 channels, whereas Ca2+ sequestration by sarco/endoplasmic reticulum Ca2+-ATPases (SERCAs) and cumulative T channel inactivation dampened oscillations. Sk2-/- (also known as Kcnn2) mice lacked cellular oscillations, showed a greater than threefold reduction in low-frequency rhythms in the electroencephalogram of non-rapid-eye-movement sleep and had disrupted sleep. Thus, the interplay of T channels, SK2 channels and SERCAs in nRt dendrites comprises a specialized Ca2+ signaling triad to regulate oscillatory dynamics related to sleep.
    Nature Neuroscience 07/2008; 11(6):683-92. · 15.53 Impact Factor
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Keywords

ambient room luminosity
 
burst responses
 
delta oscillations
 
delta rhythmicity result
 
delta rhythms
 
depolarizing spindle oscillations
 
dorsal lateral geniculate cells
 
dorsal lateral geniculate neurons
 
electroencephalogram delta waves
 
internal capsule stimulation
 
optic chiasm stimulation
 
oscillating neurons
 
Perigeniculate neurons
 
perigeniculate sector
 
reticular thalamic nuclear complex
 
reticular thalamic nucleus
 
single spikes
 
two types
 
visual sector
 
visual thalamic neurons