The supramammillary nucleus and the claustrum activate the cortex during REM sleep

Renouard, Leslie; Billwiller, Francesca; Ogawa, Keiko; Olivier, C; Camargo, Nutabi; Abdelkarim, Mouaadh; Scoté-Blachon, Céline; Touré, Rouguy; Libourel, Paul-Antoine; Ravassard, P.; Salvert, Denise; Peyron, Christelle; Bruno, Claudio; Léger, Lucienne; Salin, P. A.; Malleret, Gaël; Fort, Patrice; Luppi, Pierre‐Hervé

doi:10.1126/sciadv.1400177

Cited by 125 publications

(119 citation statements)

References 81 publications

(116 reference statements)

Supporting

Mentioning

107

Contrasting

Order By: Relevance

“…This is important given the influence of the supramammillary nuclei on hippocampal theta frequency (e.g., Kirk, 1998). As such, many studies that have assessed the effects of mammillary body lesions, or inactivation, on hippocampal theta can be difficult to interpret when damage extends into the overlying supramammillary nuclei (Sharp and Koester, 2008;Zakowski et al, 2017) and vice versa (Renouard et al, 2015). Nevertheless, the only previous study that has examined hippocampal theta following mammillary body manipulation in non-anesthetized animals established a similar pattern of changes to those reported here, with a reduction in hippocampal theta-frequency (Sharp and Koester, 2008).…”

Section: Discussionmentioning

confidence: 99%

Mammillothalamic disconnection alters hippocampo-cortical oscillatory activity and microstructure: Implications for diencephalic amnesia

Dillingham

Milczarek²,

Perry³

et al. 2019

Preprint

View full text Add to dashboard Cite

for technical, histological and surgical assistance. AbstractDiencephalic amnesia can be as disruptive as the more commonly known temporal lobe amnesia, yet the precise contribution of diencephalic structures to memory processes remains elusive. We used discrete lesions of the mammillothalamic tract to model aspects of diencephalic amnesia and assessed the impact of these lesions on multiple measures of activity and plasticity within the hippocampus and retrosplenial cortex. Lesions of the mammillothalamic tract had widespread indirect effects on hippocampo-cortical oscillatory activity within both theta and gamma bands. Both within-region oscillatory activity and cross-regional synchrony were altered. The network changes were state-dependent, displaying different profiles during locomotion and paradoxical sleep. Consistent with the associations between oscillatory activity and plasticity, complementary analyses using several convergent approaches revealed microstructural changes, which appeared to reflect a suppression of learning-induced plasticity in lesioned animals. Together, these combined findings suggest a mechanism by which damage to the medial diencephalon can impact upon learning and memory processes, highlighting important role for the mammillary bodies in the co-ordination of hippocampo-cortical activity.

show abstract

Section: Discussionmentioning

confidence: 99%

Mammillothalamic disconnection alters hippocampo-cortical oscillatory activity and microstructure: Implications for diencephalic amnesia

Dillingham

Milczarek²,

Perry³

et al. 2019

Preprint

View full text Add to dashboard Cite

show abstract

“…2). Unlike in the hippocampus, firing rates increased at the transition from NREM to REM (Evarts, 1964;McCarley and Hobson, 1971;Vyazovskiy et al, 2009;Renouard et al, 2015; but also see Niethard et al, 2016). However, similar to the hippocampus, firing rate distributions widened upon this transition, with higher firing neocortical cells showing relatively larger increases at the transition to REM (Δfiring rate = 24.9±5.4%, 33.3±5.7%, 34.0±4.1%, 53.9±6.7%, and 41.3±3.8%, for each quintile from last 1/3 of NREM to first 1/3 of REM, F (4) = 4.3, p = 0.002, one-way ANOVA; Fig.…”

Section: Differential Effects Of Rem and Nrem On Higher-and Lower-firmentioning

confidence: 99%

Neuronal firing rates diverge during REM and homogenize during non-REM

Miyawaki

Watson

Diba

2016

Preprint

View full text Add to dashboard Cite

Neurons fire at highly variable innate rates and recent evidence suggests that low and high firing rate neurons display different plasticity and dynamics. Furthermore, recent publications imply possibly differing rate-dependent effects in hippocampus versus neocortex, but those analyses were carried out separately and with possibly important differences. To more effectively synthesize these questions, we analyzed the firing rate dynamics of populations of neurons in both hippocampal CA1 and frontal cortex under one framework that avoids pitfalls of previous analyses and accounts for regression-to-the-mean. We observed remarkably consistent effects across these regions. While rapid eye movement (REM) sleep was marked by decreased hippocampal firing and increased neocortical firing, in both regions firing rates distributions widened during REM due to differential changes in high-firing versus low-firing cells in parallel with increased interneuron activity. In contrast, upon non-REM (NREM) sleep, firing rate distributions narrowed while interneuron firing decreased. Interestingly, hippocampal interneuron activity closely followed the patterns observed in neocortical principal cells rather than the hippocampal principal cells, suggestive of long-range interactions. Following these undulations in variance, the net effect of sleep was a decrease in firing rates. These decreases were greater in lower-firing hippocampal neurons but higher-firing frontal cortical neurons, suggestive of greater plasticity in these cell groups. Our results across two different regions and with statistical corrections indicate that the hippocampus and neocortex show a mixture of differences and similarities as they cycle between sleep states with a unifying characteristic of homogenization of firing during NREM and diversification during REM. Significance StatementMiyawaki and colleagues analyze firing patterns across low-firing and high-firing neurons in the hippocampus and the frontal cortex throughout sleep in a framework that accounts for regression-to-the-mean. They find that in both regions REM sleep activity is relatively dominated by high-firing neurons and increased inhibition, resulting in a wider distribution of firing rates. On the other hand, NREM sleep produces lower inhibition, and results in a more homogenous distribution of firing rates. Integration of these changes across sleep results in net decrease of firing rates with largest drops in low-firing hippocampal pyramidal neurons and high-firing neocortical principal neurons. These findings provide insights into the effects and functions of different sleep stages on cortical neurons.

show abstract

“…Although these neurons were identified more than 30 years ago, recent studies have demonstrated that most of these neurons contain glutamate, and that some also contain GABA [33;34]. Supramammillary neurons that project to the dentate gyrus of the hippocampus may release both neurotransmitters, and are thought to be active during REM sleep [34]. However, the cortically projecting neurons are mainly just glutamatergic, and chemogenetic activation of them strongly promotes waking [35].…”

Section: Supramammillary Glutamatergic and Gabaergic Arousal Systemmentioning

confidence: 99%

Wake–sleep circuitry: an overview

Saper

Fuller

2017

Current Opinion in Neurobiology

315

245

View full text Add to dashboard Cite

Although earlier models of brain circuitry controlling wake-sleep focused on monaminergic and cholinergic arousal systems, recent evidence indicates that these play mainly a modulatory role, and that the backbone of the wake-sleep regulatory system depends upon fast neurotransmitters, such as glutmate and GABA. We review here recent advances in understanding the role these systems play in controlling sleep and wakefulness.

show abstract

The supramammillary nucleus and the claustrum activate the cortex during REM sleep

Abstract: Plasticity and cortical activation during REM sleep is shown by a subset of cortical and hippocampal neurons.

Cited by 125 publications

References 81 publications

Mammillothalamic disconnection alters hippocampo-cortical oscillatory activity and microstructure: Implications for diencephalic amnesia

Mammillothalamic disconnection alters hippocampo-cortical oscillatory activity and microstructure: Implications for diencephalic amnesia

Neuronal firing rates diverge during REM and homogenize during non-REM

Wake–sleep circuitry: an overview

Contact Info

Product

Resources

About