Early ethanol pre-exposure alters breathing patterns by disruptions in the central respiratory network and serotonergic balance in neonate rats

Macchione, Ana Fabiola; Trujillo, Verónica; Anunziata, Florencia; Sahonero, M; Anastasía, Agustín; Abate, Paula; Molina, J. C.

doi:10.1016/j.bbr.2020.112908

Cited by 3 publications

(6 citation statements)

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“…Ethanol’s first metabolite role was assayed along with the activity of brain catalase system during this stage of development. In line with previous findings ( Cullere et al, 2015 ; Acevedo et al, 2017a ; Macchione et al, 2018 , 2021 ), we observed that early exposure to ethanol sensitizes pups to ethanol’s respiratory depressant effects upon breathing patterns and increases apneic episodes ( Figures 2A,B ). In addition, pups showed lower breathing frequencies until an apneic episode occurred (coefficient breaths/apneas, Figure 2C ).…”

Section: Discussionsupporting

confidence: 93%

“…response to low oxygen environment in neonates, infants, and adults (Dubois et al, 2006(Dubois et al, , 2008(Dubois et al, , 2013Kervern et al, 2009;Dubois and Pierrefiche, 2020). However, while effects on the respiratory system seems due to chronic exposure to ethanol, our data along with recent studies show that brief fetal and neonatal experiences with a moderate ethanol dose are sufficient to functionally disrupt the respiratory plasticity of the organisms under associative and non-associative learning processes (Cullere et al, 2015;Macchione et al, 2016Macchione et al, , 2018Macchione et al, , 2021Acevedo et al, 2017a;D'aloisio et al, 2020;Anunziata et al, 2021).…”

Section: Discussionmentioning

confidence: 45%

“…In addition, pups showed lower breathing frequencies until an apneic episode occurred (coefficient breaths/apneas, Figure 2C ). Regardless of the treatment’s nature, a transient decrease in breathing frequencies ( Figure 2A ) was observed throughout evaluations, indicative of a habituation process ( Macchione et al, 2016 , 2018 , 2021 ; Acevedo et al, 2017a , b ; D’aloisio et al, 2020 ; Trujillo et al, 2020 ). The short and long-term effects of ethanol on neonatal respiratory plasticity more recently have received attention given the association between fetal alcohol exposure and the sudden infant death syndrome ( Iyasu et al, 2002 ; Burd et al, 2004 ; Bailey and Sokol, 2011 ; O’Leary et al, 2013 ).…”

Section: Discussionmentioning

confidence: 99%

“…One basal minute was considerate to allow air pressure stabilization. These experimental procedures have been previously used to assess breathing patterns as function of ethanol exposure during pre- and postnatal period ( Cullere et al, 2015 ; Macchione et al, 2016 , 2018 , 2021 ; Acevedo et al, 2017a , b ; D’aloisio et al, 2020 ; Anunziata et al, 2021 ).…”

Section: Methodsmentioning

confidence: 99%

“…Such early experiences not only generate sensitivity to the positive motivational effects of ethanol but also sensitize the organism to the consequences of ethanol upon respiratory plasticity. Brief experiences with moderate doses of ethanol during late gestation (Cullere et al, 2015) or within the first postnatal week that generate respiratory disruptions indicative of sensitization processes (Cullere et al, 2015;Macchione et al, 2016Macchione et al, , 2018Macchione et al, , 2021Acevedo et al, 2017a;D'aloisio et al, 2020). Moreover, the association of a salient odor stimulus (e.g., ethanol) in the presence of ethanol-related respiratory disruptions, elicit later conditioned breathing depressions and increase the occurrence of apneic episodes (Cullere et al, 2015;Macchione et al, 2016Macchione et al, , 2018.…”

Section: Introductionmentioning

confidence: 99%

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Moderate ethanol exposure during early ontogeny of the rat alters respiratory plasticity, ultrasonic distress vocalizations, increases brain catalase activity, and acetaldehyde-mediated ethanol intake

D'aloisio

Acevedo²,

Angulo-Alcalde³

et al. 2022

Front. Behav. Neurosci.

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Early ontogeny of the rat (late gestation and postnatal first week) is a sensitive period to ethanol’s positive reinforcing effects and its detrimental effects on respiratory plasticity. Recent studies show that acetaldehyde, the first ethanol metabolite, plays a key role in the modulation of ethanol motivational effects. Ethanol brain metabolization into acetaldehyde via the catalase system appears critical in modulating ethanol positive reinforcing consequences. Catalase system activity peak levels occur early in the ontogeny. Yet, the role of ethanol-derived acetaldehyde during the late gestational period on respiration response, ultrasonic vocalizations (USVs), and ethanol intake during the first week of the rat remains poorly explored. In the present study, pregnant rats were given a subcutaneous injection of an acetaldehyde-sequestering agent (D-penicillamine, 50 mg/kg) or saline (0.9% NaCl), 30 min prior to an intragastric administration of ethanol (2.0 g/kg) or water (vehicle) on gestational days 17–20. Respiration rates (breaths/min) and apneic episodes in a whole-body plethysmograph were registered on postnatal days (PDs) 2 and 4, while simultaneously pups received milk or ethanol infusions for 40-min in an artificial lactation test. Each intake test was followed by a 5-min long USVs emission record. On PD 8, immediately after pups completed a 15-min ethanol intake test, brain samples were collected and kept frozen for catalase activity determination. Results indicated that a moderate experience with ethanol during the late gestational period disrupted breathing plasticity, increased ethanol intake, as well brain catalase activity. Animals postnatally exposed to ethanol increased their ethanol intake and exerted differential affective reactions on USVs and apneic episodes depending on whether the experience with ethanol occur prenatal or postnatally. Under the present experimental conditions, we failed to observe, a clear role of acetaldehyde mediating ethanol’s effects on respiratory plasticity or affective states, nevertheless gestational acetaldehyde was of crucial importance in determining subsequent ethanol intake affinity. As a whole, results emphasize the importance of considering the participation of acetaldehyde in fetal programming processes derived from a brief moderate ethanol experience early in development, which in turn, argues against “safe or harmless” ethanol levels of exposure.

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Section: Discussionsupporting

confidence: 93%

Section: Discussionmentioning

confidence: 45%

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Moderate ethanol exposure during early ontogeny of the rat alters respiratory plasticity, ultrasonic distress vocalizations, increases brain catalase activity, and acetaldehyde-mediated ethanol intake

D'aloisio

Acevedo²,

Angulo-Alcalde³

et al. 2022

Front. Behav. Neurosci.

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Sexual dimorphic vulnerability of respiratory control in a neonatal rodent model of fetal alcohol spectrum disorder

Rickman

Mayer

Vatolin

et al. 2023

Respiratory Physiology & Neurobiology

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Parental Preconception and Pre-Hatch Exposure to A Developmental Insult Alters Offspring’s Gene Expression and Epigenetic Regulations: An Avian Model

Rimawi¹,

Turgeman

Avital-Cohen

et al. 2023

IJMS

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Parental exposure to insults was initially considered safe if stopped before conception. In the present investigation, paternal or maternal preconception exposure to the neuroteratogen chlorpyrifos was investigated in a well-controlled avian model (Fayoumi) and compared to pre-hatch exposure focusing on molecular alterations. The investigation included the analysis of several neurogenesis, neurotransmission, epigenetic and microRNA genes. A significant decrease in the vesicular acetylcholine transporter (SLC18A3) expression was detected in the female offspring in the three investigated models: paternal (57.7%, p < 0.05), maternal (36%, p < 0.05) and pre-hatch (35.6%, p < 0.05). Paternal exposure to chlorpyrifos also led to a significant increase in brain-derived neurotrophic factor (BDNF) gene expression mainly in the female offspring (27.6%, p < 0.005), while its targeting microRNA, miR-10a, was similarly decreased in both female (50.5%, p < 0.05) and male (56%, p < 0.05) offspring. Doublecortin’s (DCX) targeting microRNA, miR-29a, was decreased in the offspring after maternal preconception exposure to chlorpyrifos (39.8%, p < 0.05). Finally, pre-hatch exposure to chlorpyrifos led to a significant increase in protein kinase C beta (PKCß; 44.1%, p < 0.05), methyl-CpG-binding domain protein 2 (MBD2; 44%, p < 0.01) and 3 (MBD3; 33%, p < 0.05) genes expression in the offspring. Although extensive studies are required to establish a mechanism–phenotype relationship, it should be noted that the current investigation does not include phenotype assessment in the offspring.

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Early ethanol pre-exposure alters breathing patterns by disruptions in the central respiratory network and serotonergic balance in neonate rats

Cited by 3 publications

References 102 publications

Moderate ethanol exposure during early ontogeny of the rat alters respiratory plasticity, ultrasonic distress vocalizations, increases brain catalase activity, and acetaldehyde-mediated ethanol intake

Moderate ethanol exposure during early ontogeny of the rat alters respiratory plasticity, ultrasonic distress vocalizations, increases brain catalase activity, and acetaldehyde-mediated ethanol intake

Sexual dimorphic vulnerability of respiratory control in a neonatal rodent model of fetal alcohol spectrum disorder

Parental Preconception and Pre-Hatch Exposure to A Developmental Insult Alters Offspring’s Gene Expression and Epigenetic Regulations: An Avian Model

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