Daily Oscillation of the Excitation-Inhibition Balance in Visual Cortical Circuits

Bridi, Morgan S.; Zong, Fang Jiao; Min, Xia; Luo, Nancy; Tran, Trinh; Qiu, Jiaqian; Severín, Daniel; Zhang, Xue Ting; Wang, Guanglin; Zhu, Ziyuan; He, Kai; Kirkwood, Alfredo

doi:10.1016/j.neuron.2019.11.011

Cited by 119 publications

(176 citation statements)

References 64 publications

(82 reference statements)

Supporting

Mentioning

156

Contrasting

Order By: Relevance

“…Moreover, E/I balance is not a static property of the cortex. It changes depending on the behavioral state (Waschke et al, 2019), task demands (Pfeffer et al, 2018;Waschke et al, 2019), performance (Sheehan et al, 2018) and depending on circadian rhythms (Bridi et al, 2020), which suggests that this property is under fine dynamic control. It has been proposed that cortical states and neural complexity could be regulated by subcortical cholinergic and noradrenergic activity (D'Andola et al, 2018); (Nghiem et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

Complexity and 1/f slope jointly reflect brain states

Medel

Irani

Ossandón

et al. 2020

Preprint

View full text Add to dashboard Cite

Characterization of cortical states is essential for understanding brain functioning in the absence of external stimuli. The balance between excitation and inhibition and the number of non-redundant activity patterns, indexed by the 1/f slope and LZc respectively, distinguish cortical states. However, the relation between these two measures has not been characterized. Here we analyzed the relation between 1/f slope and LZc with two modeling approaches and in empirical human EEG and monkey ECoG data. We contrasted resting state with propofol anesthesia, which is known to modulate the excitation-inhibition balance. We found convergent results among all strategies employed, showing an inverse and not trivial monotonic relation between 1/f slope and complexity. This behavior was observed even when the signals’ spectral properties were heavily manipulated, consistent at ECoG and EEG scales. Models also showed that LZc was strongly dependent on 1/f slope but independent of the signal’s spectral power law’s offset. Our results show that, although these measures have very distinct mathematical origins, they are closely related. We hypothesize that differentially entropic regimes could underlie the link between the excitation-inhibition balance and the vastness of repertoire of cortical systems.

show abstract

Section: Discussionmentioning

confidence: 99%

Complexity and 1/f slope jointly reflect brain states

Medel

Irani

Ossandón

et al. 2020

Preprint

View full text Add to dashboard Cite

show abstract

“…The latter conclusion also has important implications for maintenance of excitatoryinhibitory (E-I) balance during SD. Recent data suggest that E-I balance normally varies over the course of the day, in a sleep-dependent manner (Bridi et al, 2020). Furthermore, prior evidence from both whole-tissue transcriptome profiling and immunohistochemistry has suggested that SD may differentially affect connections from excitatory to inhibitory neurons (and vice versa) in structures like the neocortex (Del Cid-Pellitero et al, 2017; Puentes-Mestril and Aton, 2017).…”

Section: Discussionmentioning

confidence: 99%

“…For example, within the neocortex, fast-spiking interneurons, or neurons with greater firing rates, appear to have differential firing rate changes across periods of sleep (Clawson et al, 2018;Vyazovskiy et al, 2009). Consistent with this idea, synaptic excitatory-inhibitory (E-I) balance was recently shown to vary in neocortex over the course of the day in a sleep-dependent manner (Bridi et al, 2020). Moreover, while most neocortical neurons fire at lower rates during slow wave sleep (SWS) vs. wake, some subclasses of neocortical neurons are selectively sleep-active (Gerashchenko et al, 2008).…”

Section: Introductionmentioning

confidence: 88%

Sleep loss drives brain region- and cell type-specific alterations in ribosome-associated transcripts involved in synaptic plasticity and cellular timekeeping

Puentes-Mestril

Delorme

Wang

et al. 2020

Preprint

View full text Add to dashboard Cite

Sleep and sleep loss are thought to impact synaptic plasticity, and recent studies have shown that sleep and sleep deprivation (SD) differentially affect gene transcription and protein translation in the mammalian forebrain. However, much less is known regarding how sleep and SD affect these processes in different microcircuit elements within the hippocampus and neocortex - for example, in inhibitory vs. excitatory neurons. Here we use translating ribosome affinity purification (TRAP) and in situ hybridization to characterize the effects of sleep vs. SD on abundance of ribosome-associated transcripts in Camk2a-expressing (Camk2a+) pyramidal neurons and parvalbumin-expressing (PV+) interneurons in mouse hippocampus and neocortex. We find that while both Camk2a+ neurons and PV+ interneurons in neocortex show concurrent SD-driven increases in ribosome-associated transcripts for activity-regulated effectors of plasticity and transcriptional regulation, these transcripts are minimally affected by SD in hippocampus. Similarly we find that while SD alters several ribosome-associated transcripts involved in cellular timekeeping in neocortical Camk2a+ and PV+ neurons, effects on circadian clock transcripts in hippocampus are minimal, and restricted to Camk2a+ neurons. Taken together, our results indicate that SD effects on transcripts destined for translation are both cell type- and brain region-specific, and that these effects are substantially more pronounced in the neocortex than the hippocampus. We conclude that SD-driven alterations in the strength of synapses, excitatory-inhibitory balance, and cellular timekeeping are likely more heterogeneous than previously appreciated.Significance StatementSleep loss-driven changes in transcript and protein abundance have been used as a means to better understand the function of sleep for the brain. Here we use translating ribosome affinity purification (TRAP) to characterize changes in abundance of ribosome-associated transcripts in excitatory and inhibitory neurons in mouse hippocampus and neocortex after a brief period of sleep or sleep loss. We show that these changes are not uniform, but are generally more pronounced in excitatory neurons than inhibitory neurons, and more pronounced in neocortex than in hippocampus.

show abstract

“…An alternative possibility is that sleep propensity may be enhanced if some of the strong wake-promoting areas are inhibited, consistent with the idea that sleep represents a default state of a neural network or the whole organism (Bandarabadi et al, 2020;Krueger et al, 2013). Therefore, even if accumulation of sleep need, in some form, occurs across many distributed brain networks (Bridi et al, 2019;Bruning et al, 2019;Honda et al, 2018;Lazarus et al, 2019;Muheim et al, 2019;Noya et al, 2019;Shi and Ueda, 2018;Tatsuki et al, 2016;Williams and Naidoo, 2020), it is likely that state switching is initiated from a relatively limited set of brain circuits, which have the capacity to integrate sleep-wake history related signals with other ecological and homeostatic demands. Whilst the biological substrate of global sleep homeostasis remains unclear, the question of which brain areas are involved in encoding the time spent awake or asleep seems tractable.…”

Section: Discussionmentioning

confidence: 66%

The role of the hypothalamus in cortical arousal and sleep homeostasis

Yamagata

Kahn

Šabanović

et al. 2020

Preprint

View full text Add to dashboard Cite

Sleep and wakefulness are not simple homogenous all-or-none states, but instead are characterized by rich dynamics of brain activity across many temporal and spatial scales. Rapid global state transitions between waking and sleeping are believed to be controlled by hypothalamic circuits, but the contribution of the hypothalamus to withinstate changes of sleep and wake "intensity" remains largely unexplored. Here we show that stimulation of inhibitory neurons in the preoptic hypothalamus does not merely trigger awakening from sleep, but the resulting awake state is also characterized by increased cortical activity. This activation is associated with a faster build-up of sleep pressure, proportional to the arousal level. These findings show that hypothalamic systems thought to exclusively control global state switching, also regulate within-state "intensity", which we propose as a key intrinsic variable in shaping the architecture of sleep/wake states across the 24h day.

show abstract

Daily Oscillation of the Excitation-Inhibition Balance in Visual Cortical Circuits

Abstract: Highlights d The excitation/inhibition (E/I) ratio is dynamic across the 24h day d Fluctuations in the E/I ratio depend on sleep/wake history d E/I ratio changes are circuit specific, not uniform across all synapses

Cited by 119 publications

References 64 publications

Complexity and 1/f slope jointly reflect brain states

Complexity and 1/f slope jointly reflect brain states

Sleep loss drives brain region- and cell type-specific alterations in ribosome-associated transcripts involved in synaptic plasticity and cellular timekeeping

The role of the hypothalamus in cortical arousal and sleep homeostasis

Contact Info

Product

Resources

About