Anesthesia differentially modulates spontaneous network dynamics by cortical area and layer

Sellers, Kristin K.; Bennett, Davis; Hutt, Axel; Fröhlich, Flavio

doi:10.1152/jn.00404.2013

Cited by 69 publications

(98 citation statements)

References 86 publications

(88 reference statements)

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“…First, the use of anesthesia can be problematic (36), but it was required in our experiments because of the invasive surgery needed to access the surface of the PC (24). To address this issue, we confirmed that two different anesthetics (urethane/chlorprothixene and fentanyl/medetomidine) gave identical results.…”

Section: Discussionsupporting

confidence: 52%

Spontaneous activity in the piriform cortex extends the dynamic range of cortical odor coding

Tantirigama

Huang

Bekkers

2017

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

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Neurons in the neocortex exhibit spontaneous spiking activity in the absence of external stimuli, but the origin and functions of this activity remain uncertain. Here, we show that spontaneous spiking is also prominent in a sensory paleocortex, the primary olfactory (piriform) cortex of mice. In the absence of applied odors, piriform neurons exhibit spontaneous firing at mean rates that vary systematically among neuronal classes. This activity requires the participation of NMDA receptors and is entirely driven by bottom-up spontaneous input from the olfactory bulb. Odor stimulation produces two types of spatially dispersed, odor-distinctive patterns of responses in piriform cortex layer 2 principal cells: Approximately 15% of cells are excited by odor, and another approximately 15% have their spontaneous activity suppressed. Our results show that, by allowing odor-evoked suppression as well as excitation, the responsiveness of piriform neurons is at least twofold less sparse than currently believed. Hence, by enabling bidirectional changes in spiking around an elevated baseline, spontaneous activity in the piriform cortex extends the dynamic range of odor representation and enriches the coding space for the representation of complex olfactory stimuli.T he brain remains intensely active even under conditions when overt external stimuli are absent (1). At first glance this behavior can seem puzzling. Pyramidal neurons in primary sensory neocortex, for example, typically fire spontaneously at approximately 1 Hz when the relevant stimuli are not present (2), raising the possibility that this background activity is noise that must be mitigated by signal averaging (3). On the other hand, spontaneous cortical activity is often structured (4) and can reflect the global state of the animal (5), suggesting that it is not simply an impediment but may serve a useful computational role. Indeed, such activity may be important for gating sensory inputs (4, 6), establishing and maintaining sensory maps (7-9), and extending the dynamic range of sensory-evoked responses (10, 11). The significance of spontaneous activity is also supported by theoretical studies showing that it emerges naturally from balanced neural networks with desirable information-processing characteristics (9, 12).Given that spontaneous spiking is likely to be a key element of cortical function, it is important to study its prevalence and properties in different cortical areas. The piriform cortex (PC) is a sensory paleocortex in mammals that is critical for recognizing and remembering odors (13-17). The PC offers a number of advantages for the study of neural information processing, including a simple trilaminar architecture and well-defined afferent input from the olfactory bulb (OB) (16, 17). As a phylogenetically "old" structure, the PC is also likely to express canonical cortical circuits that have been conserved across evolution (18). Spontaneous spiking has been reported in the PC of rodents breathing odor-free air (19-23), but these studies used unit r...

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Section: Discussionsupporting

confidence: 52%

Spontaneous activity in the piriform cortex extends the dynamic range of cortical odor coding

Tantirigama

Huang

Bekkers

2017

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

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“…Recently, the cortical layer-specific effects of isoflurane plus xylazine on spontaneous LFP and multiunit activity (MUA) were examined in a ferret model (Sellers et al, 2013). Isoflurane at 0.5% and 0.75% concentration increased MUA in layer IV of visual cortex but decreased it in superficial and deep layers.…”

Section: Discussionmentioning

confidence: 99%

“…However, more systematic testing with similar grid-type microelectrode arrays as used here will be required to support this preliminary conclusion. In fact, region-specific differences in the responses of LFP and MUA to isoflurane between visual and prefrontal cortex have been recently observed (Sellers et al, 2013). In prefrontal cortex, the laminar changes were rather uniform and the LFP correlations were increased with isoflurane (the opposite to that seen in visual cortex).…”

Section: Discussionmentioning

confidence: 99%

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Graded defragmentation of cortical neuronal firing during recovery of consciousness in rats

et al. 2014

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State-dependent neuronal firing patterns reflect changes in ongoing information processing and cortical function. A disruption of neuronal coordination has been suggested as the neural correlate of anesthesia. Here, we studied the temporal correlation patterns of ongoing spike activity, during a stepwise reduction of the volatile anesthetic desflurane, in the cerebral cortex of freely moving rats. We hypothesized that the recovery of consciousness from general anesthesia is accompanied by specific changes in the spatiotemporal pattern and correlation of neuronal activity. Sixty-four contact microelectrode arrays were chronically implanted in primary visual cortex (contacts spanning 1.4 mm depth and 1.4 mm width) for recording of extracellular unit activity at four steady-state levels of anesthesia (8%–2% desflurane) and wakefulness. Recovery of consciousness was defined as the regaining of the righting reflex (near 4%). High-intensity firing (HI) periods were segmented using a threshold (200 ms) representing the minimum in the neurons’ bimodal interspike interval histogram under anesthesia. We found that the HI periods were highly fragmented in deep anesthesia and gradually transformed to a near-continuous firing pattern at wakefulness. As the anesthetic was withdrawn, HI periods became longer and increasingly correlated among the units both locally and across remote recording sites. Paradoxically, in 4 of 8 animals, HI correlation was also high at the deepest level of anesthesia (8%) when local field potentials (LFP) were burst-suppressed. We conclude that recovery from desflurane anesthesia is accompanied by a graded defragmentation of neuronal activity in the cerebral cortex. Hypersynchrony during deep anesthesia is an exception that occurs only with LFP burst suppression.

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“…Clinically relevant concentrations of propofol cause specific changes in electroencephalogram (EEG) rhythms of healthy adult humans. Up to sedative concentrations, these observations include an increase in power in the α− (at about 10 Hz) and δ− (at about 3 Hz) frequency bands over the frontal head region, accompanied by decreased α−activity, and an increase in δ−activity over the occipital sites (Murphy et al 2011;Ching et al2010;Feshchenko et al 2004;Hazeaux et al 1987;Sellers et al 2013). It has been shown that in deeper sedation propofol attenuates posterior α− power and increases frontal β and total power (Cimenser et al 2011;Gugino et al 2001) and is associated with a frontal increase in α−, δ−, and θ −power.…”

Section: Introductionmentioning

confidence: 99%

How the cortico-thalamic feedback affects the EEG power spectrum over frontal and occipital regions during propofol-induced sedation

2015

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Increasing concentrations of the anaesthetic agent propofol initially induces sedation before achieving full general anaesthesia. During this state of anaesthesia, the observed specific changes in electroencephalographic (EEG) rhythms comprise increased activity in the δ- (0.5-4 Hz) and α- (8-13 Hz) frequency bands over the frontal region, but increased δ- and decreased α-activity over the occipital region. It is known that the cortex, the thalamus, and the thalamo-cortical feedback loop contribute to some degree to the propofol-induced changes in the EEG power spectrum. However the precise role of each structure to the dynamics of the EEG is unknown. In this paper we apply a thalamo-cortical neuronal population model to reproduce the power spectrum changes in EEG during propofol-induced anaesthesia sedation. The model reproduces the power spectrum features observed experimentally both in frontal and occipital electrodes. Moreover, a detailed analysis of the model indicates the importance of multiple resting states in brain activity. The work suggests that the α-activity originates from the cortico-thalamic relay interaction, whereas the emergence of δ-activity results from the full cortico-reticular-relay-cortical feedback loop with a prominent enforced thalamic reticular-relay interaction. This model suggests an important role for synaptic GABAergic receptors at relay neurons and, more generally, for the thalamus in the generation of both the δ- and the α- EEG patterns that are seen during propofol anaesthesia sedation.

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Anesthesia differentially modulates spontaneous network dynamics by cortical area and layer

Cited by 69 publications

References 86 publications

Spontaneous activity in the piriform cortex extends the dynamic range of cortical odor coding

Spontaneous activity in the piriform cortex extends the dynamic range of cortical odor coding

Graded defragmentation of cortical neuronal firing during recovery of consciousness in rats

How the cortico-thalamic feedback affects the EEG power spectrum over frontal and occipital regions during propofol-induced sedation

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