Spatiotemporal patterns of neocortical activity around hippocampal sharp-wave ripples

Abadchi, Javad Karimi; Nazari-Ahangarkolaee, Mojtaba; Gattas, Sandra; Bermudez-Contreras, Edgar; Luczak, Artur; McNaughton, Bruce L.; Mohajerani, Majid H.

doi:10.7554/elife.51972

Cited by 113 publications

(128 citation statements)

References 86 publications

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“…In this view, the higher accumulation of angles at 0 degrees observed when comparing force vs non force events could represent the hallmark of such network switch. Interestingly, a similar propagation pattern has been observed applying optical flow analysis to calcium imaging over the same cortical areas when windowing cortical activity around hippocampal sharp wave ripples during sleep (Karimi Abadchi et al, 2020) and corresponds to one of the two major propagation patterns observed during slow wave sleep (Greenberg et al, 2018). Our findings extend these results to the awake condition during motor execution.…”

Section: Cortical Propagation Features In Healthy Micesupporting

confidence: 82%

Cortical propagation as a biomarker for recovery after stroke

Cecchini

Scaglione

Mascaro

et al. 2020

Preprint

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Stroke is a debilitating condition which affects millions of people worldwide. The development of improved rehabilitation paradigms rests on finding biomarkers suitable for tracking functional damage and recovery. We perform a detailed spatiotemporal analysis of wide-field calcium images from mice during longitudinal motor training before and after focal stroke induction. We define three indicators that characterise the duration, the angle of propagation and the smoothness of global movement-evoked activation patterns. During acute stroke we observe an increase in global event duration and a decrease in smoothness over the ipsilesional hemisphere. For both rehabilitation via motor training alone and combined with pharmacological therapy, we find clear signs of recovery, but surprisingly, cortical propagation in double treated mice with generalised recovery is even faster and smoother than before stroke. Our propagation-based biomarkers deliver unforeseen insight into brain mechanisms underlying motor recovery and thus pave the way towards a more targeted post-stroke therapy.

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Section: Cortical Propagation Features In Healthy Micesupporting

confidence: 82%

Cortical propagation as a biomarker for recovery after stroke

Cecchini

Scaglione

Mascaro

et al. 2020

Preprint

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“…Glutamate is an important neurotransmitter that regulates neural activity and cerebral metabolism during wakefulness and sleep. However, much of the previous work studying extracellular release has been done using fixed-potential amperometry 43 , or optical imaging in head-fixed mice 44 . Inducing sleep in head-fixed mice is challenging and typically requires sleep deprivation which can alter the overall sleep structure and patterns of rapid eye-movement (REM) and non-REM (NREM) sleep 45,46 .…”

Section: Imaging Glutamate Release Dynamics During Wakefulness and Namentioning

confidence: 99%

“…Inducing sleep in head-fixed mice is challenging and typically requires sleep deprivation which can alter the overall sleep structure and patterns of rapid eye-movement (REM) and non-REM (NREM) sleep 45,46 . The design flexibility of the See-Shells allowed us to incorporate local field potential (LFP) recording electrodes in the dorsal hippocampus in Emx-CaMKII-Ai85 mice, expressing iGluSnFR in glutamatergic neocortical neurons 33,44,47 . Mice were allowed to naturally transition to sleep in their home cage.…”

Section: Imaging Glutamate Release Dynamics During Wakefulness and Namentioning

confidence: 99%

Miniaturized head-mounted device for whole cortex mesoscale imaging in freely behaving mice

Rynes

Surinach

Linn

et al. 2020

Preprint

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The advent of genetically encoded calcium indicators, along with surgical preparations such as thinned skulls or refractive index matched skulls, have enabled mesoscale cortical activity imaging in head-fixed mice. Such imaging studies have revealed complex patterns of coordinated activity across the cortex during spontaneous behaviors, goal-directed behavior, locomotion, motor learning, and perceptual decision making. However, neural activity during unrestrained behavior significantly differs from neural activity in head-fixed animals. Whole-cortex imaging in freely behaving mice will enable the study of neural activity in a larger, more complex repertoire of behaviors not possible in head-fixed animals. Here we present the “Mesoscope,” a wide-field miniaturized, head-mounted fluorescence microscope compatible with transparent polymer skulls recently developed by our group. With a field of view of 8 mm x 10 mm and weighing less than 4 g, the Mesoscope can image most of the mouse dorsal cortex with resolution ranging from 39 to 56 µm. Stroboscopic illumination with blue and green LEDs allows for the measurement of both fluorescence changes due to calcium activity and reflectance signals to capture hemodynamic changes. We have used the Mesoscope to successfully record mesoscale calcium activity across the dorsal cortex during sensory-evoked stimuli, open field behaviors, and social interactions. Finally, combining the mesoscale imaging with electrophysiology enabled us to measure dynamics in extracellular glutamate release in the cortex during the transition from wakefulness to natural sleep.

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“…Therefore, SWR interval is not likely the cause of the differential post-SWR cortical activity pattern in ENR. Of note, we also analyzed urethane anesthetized mice (Karimi Abadchi et al, 2020) and found that results were distinct to natural sleeping mice regardless of rearing conditions (ISO, normal caged mice (NOR), and ENR; Figure 4). The results suggest that the distinct activity patterns between awake and sleep state are likely to be caused by natural awake/sleep cycles.…”

Section: Resultsmentioning

confidence: 99%

Brain state-dependent cortico-hippocampal network dynamics are modulated by postnatal stimuli

Shinohara

Koketsu

Hirase

et al. 2020

Preprint

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Neurons in the cerebral cortex and hippocampus discharge synchronously in a brain state-dependent manner to transfer information. Published studies have highlighted the temporal coordination of neuronal activities between the hippocampus and a cortical area, however, how the spatial extent of cortex activity relates to hippocampal activity remains largely unknown. We imaged macroscopic cortical activity while recording hippocampal local field potentials in unanesthetized GCaMP-expressing transgenic mice. We found that cortical activity elevates before and after hippocampal sharp wave ripples (SWR). SWR-associated cortical activities occurred predominantly in vision-related regions including visual, retrosplenial and prefrontal cortex. While pre-SWR cortical activities were frequently observed in awake and sleep states, post-SWR cortical activity decreased significantly in sleep. During hippocampal theta oscillation states, phase-locked oscillations of calcium activity was observed throughout the entire cortex state. Environmental effects on cortico-hippocampal dynamics were also assessed by comparing mice reared in an enriched environment (ENR) or under isolated conditions (ISO). In both SWR and theta oscillations, mice reared in an isolated condition exhibited clearer brain state-dependent dynamics than those reared in an enriched environment. Our data demonstrate that the cortex and hippocampus exhibit heterogeneous activity patterns that characterize brain states, and postnatal experience plays a significant role in modulating these patterns.Significant StatementThe hippocampus is a center for memory formation. However, the memory formed in the hippocampus is not stored forever, but gradually transferred into the cerebral cortex. As an underlying mechanism, phase-locked synchronized activities between the cortex and hippocampus has been hypothesized. However, spatio-temporal dynamics between hippocampus and whole cortical areas remained mostly unknown. We measured cortical calcium activities with hippocampal electroencephalogram (EEG) simultaneously, and found that the activities of widespread cortical areas are temporally associated with hippocampal EEG. The cortico-hippocampal dynamics is primarily regulated by animal awake/sleep state. Even if similar EEG patters were observed, temporal dynamics between the cortex and hippocampus exhibit distinct patterns between awake and sleep period. In addition, animals’ postnatal experience modulates the dynamics.

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Spatiotemporal patterns of neocortical activity around hippocampal sharp-wave ripples

Cited by 113 publications

References 86 publications

Cortical propagation as a biomarker for recovery after stroke

Cortical propagation as a biomarker for recovery after stroke

Miniaturized head-mounted device for whole cortex mesoscale imaging in freely behaving mice

Brain state-dependent cortico-hippocampal network dynamics are modulated by postnatal stimuli

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