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Effects of neonatal isoflurane anesthesia exposure on learning-specific and sensory systems in adults.

ABSTRACT: Millions of children undergo general anesthesia each year, and animal and human studies have indicated that exposure to anesthesia at an early age can impact neuronal development, leading to behavioral and learning impairments that manifest later in childhood and adolescence. Here, we examined the effects of isoflurane, a commonly-used general anesthetic, which was delivered to newborn rabbits. Trace eyeblink classical conditioning was used to assess the impact of neonatal anesthesia exposure on behavioral learning in adolescent subjects, and a variety of MRI techniques including fMRI, MR volumetry, spectroscopy and DTI captured functional, metabolic, and structural changes in key regions of the learning and sensory systems associated with anesthesia-induced learning impairment. Our results demonstrated a wide array of changes that were specific to anesthesia-exposed subjects, which supports previous studies that have pointed to a link between early anesthesia exposure and the development of learning and behavioral deficiencies. These findings point to the need for caution in avoiding excessive use of general anesthesia in young children and neonates.

SUBMITTER: Aksenov DP

PROVIDER: S-EPMC7429916 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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Effects of neonatal isoflurane anesthesia exposure on learning-specific and sensory systems in adults.

Aksenov Daniil P DP Venkatasubramanian Palamadai N PN Miller Michael J MJ Dixon Conor J CJ Li Limin L Wyrwicz Alice M AM

Scientific reports 20200814 1

Millions of children undergo general anesthesia each year, and animal and human studies have indicated that exposure to anesthesia at an early age can impact neuronal development, leading to behavioral and learning impairments that manifest later in childhood and adolescence. Here, we examined the effects of isoflurane, a commonly-used general anesthetic, which was delivered to newborn rabbits. Trace eyeblink classical conditioning was used to assess the impact of neonatal anesthesia exposure on ...[more]

PMID: 32796946

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Project description:The disruption of coupling between brain areas has been suggested as the mechanism underlying loss of consciousness in anesthesia. This hypothesis has been tested previously by measuring the information transfer between brain areas, and by taking reduced information transfer as a proxy for decoupling. Yet, information transfer is a function of the amount of information available in the information source-such that transfer decreases even for unchanged coupling when less source information is available. Therefore, we reconsidered past interpretations of reduced information transfer as a sign of decoupling, and asked whether impaired local information processing leads to a loss of information transfer. An important prediction of this alternative hypothesis is that changes in locally available information (signal entropy) should be at least as pronounced as changes in information transfer. We tested this prediction by recording local field potentials in two ferrets after administration of isoflurane in concentrations of 0.0%, 0.5%, and 1.0%. We found strong decreases in the source entropy under isoflurane in area V1 and the prefrontal cortex (PFC)-as predicted by our alternative hypothesis. The decrease in source entropy was stronger in PFC compared to V1. Information transfer between V1 and PFC was reduced bidirectionally, but with a stronger decrease from PFC to V1. This links the stronger decrease in information transfer to the stronger decrease in source entropy-suggesting reduced source entropy reduces information transfer. This conclusion fits the observation that the synaptic targets of isoflurane are located in local cortical circuits rather than on the synapses formed by interareal axonal projections. Thus, changes in information transfer under isoflurane seem to be a consequence of changes in local processing more than of decoupling between brain areas. We suggest that source entropy changes must be considered whenever interpreting changes in information transfer as decoupling.

Project description:INTRODUCTION:Correlated low-frequency fluctuations of resting-state functional magnetic resonance imaging (rsfMRI) signals have been widely used for inferring intrinsic brain functional connectivity (FC). In animal studies, accurate estimate of anesthetic effects on rsfMRI signals is demanded for reliable interpretations of FC changes. We have previously shown that inter-regional FC can reliably delineate local millimeter-scale circuits within digit representations of primary somatosensory cortex (S1) subregions (areas 3a, 3b, and 1) in monkeys under isoflurane anesthesia. The goals of this study are to determine (1) the general effects of isoflurane on rsfMRI signals in the S1 circuit and (2) whether the effects are functional- and regional- dependent, by quantifying the relationships between isoflurane levels, power and inter-regional correlation coefficients in digit and face regions of distinct S1 subregions. METHODS:Functional MRI data were collected from male adult squirrel monkeys at three different isoflurane levels (1.25%, 0.875%, and 0.5%). All scans were acquired on a 9.4T magnet with a 3-cm-diameter surface transmit-receive coil centered over the S1 cortex. Power and seed-based inter-regional functional connectivity analyses were subsequently performed. RESULTS:As anesthesia level increased, we observed (1) diminishing amplitudes of signal fluctuations, (2) reduced power of fluctuations in the low-frequency band used for connectivity measurements, (3) decreased inter-voxel connectivity around seed regions, and (4) weakened inter-regional FC across all pairs of regions of interest (digit-to-digit). The low-frequency power measures derived from rsfMRI signals from control muscle regions, however, did not exhibit any isoflurane level-related changes. Within the isoflurane dosage range we tested, the inter-regional functional connectivity differences were still detectable, and the effects of isoflurane did not differ across region-of-interest (ROI) pairs. CONCLUSION:Our data demonstrate that isoflurane induced similar dose-dependent suppressive effects on the power of rsfMRI signals and local fine-scale FC across functionally related but distinct S1 subregions.

Dataset Information

Effects of neonatal isoflurane anesthesia exposure on learning-specific and sensory systems in adults.

Publications

Effects of neonatal isoflurane anesthesia exposure on learning-specific and sensory systems in adults.

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