The slow (< 1 Hz) oscillation in reticular thalamic and thalamocortical neurons: scenario of sleep rhythm generation in interacting thalamic and neocortical networks

Abstract

As most afferent axons to the thalamus originate in the cerebral cortex, we assumed that the slow (< 1 Hz) cortical oscillation described in the two companion articles is reflected in reticular (RE) thalamic and thalamocortical cells. We hypothesized that the cortically generated slow rhythm would appear in the thalamus in conjunction with delta and spindle oscillations arising from intrinsic and network properties of thalamic neurons. Intracellular recordings have been obtained in anesthetized cats from RE (n = 51) and cortically projecting (n = 240) thalamic neurons. RE cells were physiologically identified by cortically evoked high-frequency spike bursts and depolarizing spindle oscillations. Thalamocortical cells were recognized by backfiring from appropriate neocortical areas, spindle-related cyclic IPSPs, and hyperpolarization-activated delta oscillation consisting of rhythmic low-threshold spikes (LTSs) alternating with afterhyperpolarizing potentials (AHPs). The slow rhythm (0.3-0.5 Hz) was recorded in 65% of RE neurons. In approximately 90% of oscillating cells, the rhythm consisted of prolonged depolarizations giving rise to trains of single action potentials. DC hyperpolarization increased the synaptic noise and, in a few cells, suppressed the long-lasting depolarizing phase of the slow rhythm, without blocking the fast EPSPs. In approximately 10% of oscillating neurons, the hyperpolarizing phase of the oscillation was much more pronounced, thus suggesting that the slow rhythm was produced by inhibitory sculpturing of the background firing. The slow oscillation was associated with faster rhythms (4-8 Hz) in the same RE neuron. The slow rhythm of RE neurons was closely related to EEG wave complexes recurring with the same frequency, and its strong dependency upon a synchronized state of cortical EEG was observed during shifts in EEG patterns at different levels of anesthesia. In 44% of thalamocortical cells the slow rhythm of depolarizing sequences was apparent and it could coexist with delta or spindle oscillations in the same neuron. The occurrence of the slowly recurring depolarizing envelopes was delayed by the hyperpolarizing spindle sequences or by the LTS-AHP sequences of delta oscillation. The hyperpolarization-activated delta potentials that tended to dampen after a few cycles were grouped in sequences recurring with the slow rhythm. We finally propose a unified scenario of the genesis of the three major sleep rhythms: slow, delta, and spindle oscillations.

The increase in medial prefrontal glutamate/glutamine concentration during memory encoding is associated with better memory performance and stronger functional connectivity in the human medial prefrontal–thalamus–hippocampus network

“…With respect to the functional connectivity to the dorsal margin of the thalamus, albeit speculative, one may assume that this thalamic region represents the thalamic reticular nucleus (Viviano and Schneider, 2015; Zikopoulos and Barbas, 2006; Jones, 1985), a layer of GABAergic cells wrapping the dorsolateral segments of the thalamus (Jones, 1985; Zikopoulos and Barbas, 2006). GABAergic neurons in the thalamic reticular nucleus modulate both corticothalamic and thalamocortical communications (Slotnick, Moo, Kraut, Lesser, & Hart, 2002; Lozsádi, 1995; Steriade, Contreras, Curró Dossi, & Nuñez, 1993; Jones, 1985). For instance, the thalamic reticular nucleus receives excitatory inputs from cortex and other thalamic nuclei and sends inhibitory projections (GABAergic) back to thalamic nuclei thereby controlling the activity/oscillations in thalamocortical loops (Slotnick et al, 2002; Lozsádi, 1995; Steriade et al,1993).…”

“…GABAergic neurons in the thalamic reticular nucleus modulate both corticothalamic and thalamocortical communications (Slotnick, Moo, Kraut, Lesser, & Hart, 2002; Lozsádi, 1995; Steriade, Contreras, Curró Dossi, & Nuñez, 1993; Jones, 1985). For instance, the thalamic reticular nucleus receives excitatory inputs from cortex and other thalamic nuclei and sends inhibitory projections (GABAergic) back to thalamic nuclei thereby controlling the activity/oscillations in thalamocortical loops (Slotnick et al, 2002; Lozsádi, 1995; Steriade et al,1993). Brain oscillations result in synaptic plasticity via synchronizing and desynchronizing neural assemblies and are therefore one of the core mechanisms underlying episodic memory (Hanslmayr, Staresina, & Bowman, 2016).…”

Spikes, synchrony, and attentive learning by laminar thalamocortical circuits

“…TRN projections to the intralaminar and midline nuclei are more diffuse than the reticular projection to the specific dorsal thalamic nuclei. The TRN influences the sleep/wake cycle (Steriade et al, 1993), the efficacy of thalamic inputs to the cortex (Nicolelis and Fanselow, 2002;Swadlow et al, 2002), and attention (Sherman and Guillery, 2001). …”

Integrated Brain Circuits: Neuron-Astrocyte Interaction in Sleep-Related Rhythmogenesis

“…Pioneering work by Steriade and colleagues has shown that identified neurons in a number of different cortical areas fluctuate between depolarized (UP) and hyperpolarized (DOWN) states[29,30,31]. The UP state is characterized by barrages of synaptic activity, a plateau depolarization, and action potential firing, while the DOWN state is characterized by cell hyperpolarization and silence[30] (Fig.…”

“…In SWS, the thalamocortical system is dominated by stereotyped field potential oscillations in the 0.5- to 4-Hz frequency range, which includes the slow (<1 Hz) oscillation and delta frequencies (1–4 Hz). Analytically described by Steriade and colleagues 17 years ago[29,30,31], the slow oscillation is now thought to be one of the primary organizers of network activity in the thalamocortical system[32] and possibly the key player in off-line memory consolidation during sleep[10,21,26]. In the remainder of this review, we will first discuss the neuronal mechanisms underlying slow oscillations, highlighting the role of dynamic cortico- and thalamocortical coupling to generate this network activity.…”