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Rhythmic dendritic Ca 2+ oscillations in thalamocortical neurons during slow non‐REM sleep‐related activity in vitro
Author(s) -
Errington Adam C.,
Hughes Stuart W.,
Crunelli Vincenzo
Publication year - 2012
Publication title -
the journal of physiology
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.802
H-Index - 240
eISSN - 1469-7793
pISSN - 0022-3751
DOI - 10.1113/jphysiol.2012.232132
Subject(s) - rhythm , sleep (system call) , neuroscience , in vitro , psychology , biology , communication , physics , medicine , computer science , biochemistry , operating system
Key points• Sensory thalamocortical (TC) neurons are thought to play a crucial role in oscillatory brain activity typical of slow wave sleep. • Intrinsic oscillations in TC neurons rely upon expression of T‐type voltage gated Ca 2+ channels. • We show that during sleep like firing patterns in TC neurons in brain slices, low threshold spikes mediated by T‐type channels produce global and rhythmic dendritic Ca 2+ signals. In particular we show Ca 2+ elevations in dendritic spine like structures during slow oscillatory activity. • We find that the duration of dendritic Ca 2+ signals and the mean level of Ca 2+ in TC neuron dendrites varies with oscillation frequency. • This global repetitive Ca 2+ entry in to TC cells during oscillations could have significant implications for synaptic signalling and biochemical processes in these important sensory neurons.Abstract The distribution of T‐type Ca 2+ channels along the entire somatodendritic axis of sensory thalamocortical (TC) neurons permits regenerative propagation of low threshold spikes (LTS) accompanied by global dendritic Ca 2+ influx. Furthermore, T‐type Ca 2+ channels play an integral role in low frequency oscillatory activity (<1–4 Hz) that is a defining feature of TC neurons. Nonetheless, the dynamics of T‐type Ca 2+ channel‐dependent dendritic Ca 2+ signalling during slow sleep‐associated oscillations remains unknown. Here we demonstrate using patch clamp recording and two‐photon Ca 2+ imaging of dendrites from cat TC neurons undergoing spontaneous slow oscillatory activity that somatically recorded δ (1–4 Hz) and slow (<1 Hz) oscillations are associated with rhythmic and sustained global oscillations in dendritic Ca 2+ . In addition, our data reveal the presence of LTS‐dependent Ca 2+ transients (Δ[Ca 2+ ]) in dendritic spine‐like structures on proximal TC neuron dendrites during slow (<1 Hz) oscillations whose amplitudes are similar to those observed in the dendritic shaft. We find that the amplitude of oscillation associated Δ[Ca 2+ ] do not vary significantly with distance from the soma whereas the decay time constant (τ decay ) of Δ[Ca 2+ ] decreases significantly in more distal dendrites. Furthermore, τ decay of dendritic Δ[Ca 2+ ] increases significantly as oscillation frequency decreases from δ to slow frequencies where pronounced depolarised UP states are observed. Such rhythmic dendritic Ca 2+ entry in TC neurons during sleep‐related firing patterns could be an important factor in maintaining the oscillatory activity and associated biochemical signalling processes, such as synaptic downscaling, that occur in non‐REM sleep.