Oscillatory patterns in hippocampus under light and deep isoflurane anesthesia closely mirror prominent brain states in awake animals

Lustig, Brian R.; Wang, Yingxue; Pastalkova, Eva

doi:10.1002/hipo.22494

Cited by 20 publications

(28 citation statements)

References 56 publications

(89 reference statements)

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“…Whereas we observed increased hippocampal delta oscillations, hippocampal delta activities have been observed so far only in primates and humans but not rodents (64,65). Previous studies in rodents showed that theta-like oscillations in the hippocampus shifted to lower frequencies (i.e., delta range) during light anesthesia (∼1.0% isoflurane) (66,67). This finding suggests that our increased delta oscillation results might arise from increased theta-like oscillations after low-frequency stimulation.…”

Section: Discussioncontrasting

confidence: 64%

“…An EEG study in humans reported EEG differences under anesthesia and sleep/wake conditions, but the authors observed sleep oscillations (i.e., slow and delta dominant) under anesthesia (80). Such oscillations were also found in rodent studies during extracellular and/or intracellular recordings (67,81,82). Taken together, these studies highlight the robust presence of lowfrequency activity in brain-wide interactions under various states, including anesthetized and sleep conditions.…”

Section: Discussionmentioning

confidence: 78%

“…Hippocampal-cortical activity is state dependent, so the light anesthesia used here may alter their characteristics (34,66,67,79). Nevertheless, prior work revealed synchronized interhemispheric delta oscillations as a major contributor to infraslow rsfMRI connectivity in anesthetized rodents (16,17).…”

Section: Discussionmentioning

confidence: 91%

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Low-frequency hippocampal–cortical activity drives brain-wide resting-state functional MRI connectivity

Chan

Leong

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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The hippocampus, including the dorsal dentate gyrus (dDG), and cortex engage in bidirectional communication. We propose that low-frequency activity in hippocampal-cortical pathways contributes to brain-wide resting-state connectivity to integrate sensory information. Using optogenetic stimulation and brain-wide fMRI and resting-state fMRI (rsfMRI), we determined the large-scale effects of spatiotemporal-specific downstream propagation of hippocampal activity. Low-frequency (1 Hz), but not high-frequency (40 Hz), stimulation of dDG excitatory neurons evoked robust cortical and subcortical brain-wide fMRI responses. More importantly, it enhanced interhemispheric rsfMRI connectivity in various cortices and hippocampus. Subsequent local field potential recordings revealed an increase in slow oscillations in dorsal hippocampus and visual cortex, interhemispheric visual cortical connectivity, and hippocampal-cortical connectivity. Meanwhile, pharmacological inactivation of dDG neurons decreased interhemispheric rsfMRI connectivity. Functionally, visually evoked fMRI responses in visual regions also increased during and after low-frequency dDG stimulation. Together, our results indicate that low-frequency activity robustly propagates in the dorsal hippocampal-cortical pathway, drives interhemispheric cortical rsfMRI connectivity, and mediates visual processing.hippocampus | resting-state functional connectivity | optogenetic | fMRI | low frequency T he hippocampus (HP) plays a prominent role in central nervous system functions, particularly in episodic memory (1, 2) and spatial navigation (3, 4). The HP, including the dentate gyrus (DG), can evoke large-scale influences on cortical activity, because the HP receives convergent information from sensory and limbic cortices before sending reciprocal divergent projections to create a highly interactive corticohippocampal-cortical network. The HP, including DG, CA3, and CA1, and neocortex, are connected via the entorhinal cortex (EC) (5, 6), such that the dorsolateral-to-ventromedial projection that originates in the EC corresponds to a dorsoventral axis of termination in the HP (5). This anatomical topography suggests that a functional gradient could exist along the HP dorsoventral axis. Previous studies demonstrated that dorsal HP (dHP) and cortex are functionally integrated during sensory processing and memory consolidation (7-9). Specifically, dHP can integrate multimodal sensory information and process memory operations (7) using excitatory longrange projections (10). This process occurs over multiple brain circuits, but the role of dHP in complex networks, particularly its influence on brain-wide functional connectivity, is not well understood.Resting-state functional MRI (rsfMRI) (11-14) provides an invaluable, noninvasive imaging technique to map long-range, brain-wide functional connectivity networks based on the temporal coherence of infraslow (0.005-0.1 Hz) blood oxygen level dependent (BOLD) activity. The functional relevance of specific brain-wide networks in co...

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Section: Discussioncontrasting

confidence: 64%

Section: Discussionmentioning

confidence: 78%

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Low-frequency hippocampal–cortical activity drives brain-wide resting-state functional MRI connectivity

Chan

Leong

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…There is also evidence that adequate depth of isoflurane anesthesia can drive the rodent hippocampus into a SPW-like state with bursts of inputs into stratum radiatum that demonstrate a similar pattern to CA3-derived SPW observed in the awake rodent (Lustig et al, 2015). We also observe regular bursts of synchronized input into stratum radiatum in the isoflurane anesthetized pig that have the typical phase reversal across the pyramidal cell layer expected of CA3-derived SPWs.…”

Section: Discussionsupporting

confidence: 64%

“…These waves demonstrated a phase reversal at the pyramidal layer, at the bottom of stratum radiatum reminiscent of sharp waves described in the awake rodent hippocampus (Bragin et al, 1995b;Buzsáki et al, 2003), and again at dentate gyrus middle molecular layer (arrows). It is possible that these are regular sharp-wave-like (SPWlike) events representing synchronized pre-synaptic currents from CA3 projections, as SPW have been shown to take on an oscillatory characteristic under isoflurane anesthesia in rodents (Lustig et al, 2015).…”

Section: Simultaneous Laminar Field Potentials and Single Unit Activimentioning

confidence: 99%

Electrophysiological Signature Reveals Laminar Structure of the Porcine Hippocampus

Ulyanova

Koch

Grovola

et al. 2017

Preprint

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The hippocampus is involved in aspects of both working and episodic memory, and is a central region of interest in diseases affecting these processes. While the role of the hippocampus in memory is studied predominantly in rodents, rodent neurological disease models have not historically translated well to human treatment. Non-human primate disease models, while highly translational, present both economic and ethical challenges. Therefore, an alternative research model is required to study memory and cognition during development and to follow disease progression. Because pig models are widely used in other translational research, they may provide an excellent compromise between rodents and non-human primates due in part to the gyrencephalic neuroanatomy and significant white matter composition of the porcine brain.In addition, the porcine hippocampal anatomy and cytoarchitecture more closely resembles that of primates than rodents. To advance the study of the neurophysiology of the pig hippocampus and related structures, we utilized stereotaxis combined with single-unit electrophysiological mapping to precisely place laminar silicon depth probes into the dorsal hippocampus of miniature pigs without the need for image guidance. We then implemented an in vivo, electrophysiology-based methodology to identify hippocampal layers and to examine hippocampal neurophysiology using these depth probes. This methodology allowed for the simultaneous recording of laminar field potentials and single-cell activity in multiple layers in the dorsal hippocampus. The laminar structure of dorsal hippocampus and the precise location of the probes were confirmed by electrophysiology and histopathology, eliminating the need to recover electrode tracks in future animals. This methodology allows us to investigate hippocampal electrophysiology under anesthesia, with potential expansion into awake behaving neurophysiology. Accessible neurophysiology of the pig hippocampus may allow for the development of new translational models of neurological disorders, with the possibility of evaluating the neuronal and circuitry disruptions that underlie cognitive and memory dysfunction.peer-reviewed)

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Frequency‐ and state‐dependent effects of hippocampal neural disinhibition on hippocampal local field potential oscillations in anesthetized rats

2020

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Reduced inhibitory GABA function, so‐called neural disinhibition, has been implicated in cognitive disorders, including schizophrenia and age‐related cognitive decline. We previously showed in rats that hippocampal disinhibition by local microinfusion of the GABA‐A receptor antagonist picrotoxin disrupted memory and attention and enhanced hippocampal multi‐unit burst firing recorded around the infusion site under isoflurane anesthesia. Here, we analyzed the hippocampal local field potential (LFP) recorded alongside the multi‐unit data. We predicted frequency‐specific LFP changes, based on previous studies implicating GABA in hippocampal oscillations, with the weight of evidence suggesting that disinhibition would facilitate theta and disrupt gamma oscillations. Using a new semi‐automated method based on the kurtosis of the LFP peak‐amplitude distribution as well as on amplitude envelope thresholding, we separated three distinct hippocampal LFP states under isoflurane anesthesia: “burst” and “suppression” states—high‐amplitude LFP spike bursts and the interspersed low‐amplitudeperiods—and a medium‐amplitude “continuous” state. The burst state showed greater overall power than suppression and continuous states and higher relative delta/theta power, but lower relative beta/gamma power. The burst state also showed reduced functional connectivity across the hippocampal recording area, especially around theta and beta frequencies. Overall neuronal firing was higher in the burst than the other two states, whereas the proportion of burst firing was higher in burst and continuous states than the suppression state. Disinhibition caused state‐ and frequency‐dependent LFP changes, tending to increase power at lower frequencies (<20 Hz), but to decrease power and connectivity at higher frequencies (>20 Hz) in burst and suppression states. The disinhibition‐induced enhancement of multi‐unit bursting was also state‐dependent, tending to be more pronounced in burst and suppression states than the continuous state. Overall, we characterized three distinct hippocampal LFP states in isoflurane‐anesthetized rats. Disinhibition changed hippocampal LFP oscillations in a state‐ and frequency‐dependent way. Moreover, the disinhibition‐induced enhancement of multi‐unit bursting was also LFP state‐dependent.

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Oscillatory patterns in hippocampus under light and deep isoflurane anesthesia closely mirror prominent brain states in awake animals

Cited by 20 publications

References 56 publications

Low-frequency hippocampal–cortical activity drives brain-wide resting-state functional MRI connectivity

Low-frequency hippocampal–cortical activity drives brain-wide resting-state functional MRI connectivity

Electrophysiological Signature Reveals Laminar Structure of the Porcine Hippocampus

Frequency‐ and state‐dependent effects of hippocampal neural disinhibition on hippocampal local field potential oscillations in anesthetized rats

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