Prenatal and postnatal exposure to ethanol induces changes in the shape of the dendritic spines from hippocampal CA1 pyramidal neurons of the rat

doi:10.1016/S0304-3940(00)01075-2

Neuroscience Letters

Volume 286, Issue 1, 26 May 2000, Pages 13-16

https://doi.org/10.1016/S0304-3940(00)01075-2 Get rights and content

Abstract

20%-ethanol was provided to adult female rats since a pregestational stage until weaning of the pups, and percentage proportion of thin, mushroom-shaped, stubby, or wide spines from the apical dendrite of hippocampal CA1 pyramidal cells, was counted at 15, 21, 40, and 90 days of age. By-kind-of-spine analysis revealed higher fluctuation of experimental spines, and less percentage of thin spines was observed in the ethanol-intoxicated rats concomitantly with a higher proportion of stubby or wide spines; through development. Because thin spines may propagate the synaptic potentials more efficiently than stubby or wide spines, this findings suggest that the electrical excitability and thereafter the firing pattern of those cells may be altered, due to the toxic effects of chronic ethanol ingestion.

References (17)

A. Cadete-Leite et al.
Hippocampal mossy fiber-CA3 synapsis after chronic alcohol consumption and withdrawal
Alcohol
(1989)
I. Ferrer et al.
Morphological recovery of hippocampal pyramidal neurons in the adult rat exposed in utero to ethanol
Toxicology
(1988)
Ch. Larue-Achagiotis et al.
Alcohol drinking, food and fluid intakes and body weight gain in rats
Physiol. Behav.
(1990)
L. Lescaudron et al.
Modifications in number and morphology of dendritic spines resulting from chronic ethanol consumption and withdrawal: a Golgi study in the mouse anterior and posterior hippocampus
Exp. Neurol.
(1989)
G. Stoltenburg-Didinger et al.
Fetal alcohol syndrome and mental retardation: spine distribution of pyramidal cells in prenatal alcohol exposed rat cerebral cortex, a Golgi study
Dev. Brain Res.
(1983)
R. Astrid et al.
Spine morphology of neurons in the avian forebrain is affected by rearing conditions
Behav. Neural. Biol.
(1994)
E.L. Crow et al.
L.D. Davies et al.
A Golgi study of mouse hippocampal CA1 piramidal neurons followings perinatal ethanol exposure
Neurosci. Lett.
(1981)

There are more references available in the full text version of this article.

Cited by (57)

Sexual experience induces a preponderance of mushroom spines in the medial prefrontal cortex and nucleus accumbens of male rats
2023, Behavioural Brain Research
Sexual experience improves copulatory performance in male rats. Copulatory performance has been associated with dendritic spines density in the medial prefrontal cortex (mPFC) and nucleus accumbens (NAcc), structures involved in the processing of sexual stimuli and the manifestation of sexual behavior. Dendritic spines modulate excitatory synaptic contacts, and their morphology is associated with the ability to learn from experience. This study was designed to determine the effect of sexual experience on the density of different types or shapes of dendritic spines in the mPFC and NAcc of male rats. A total of 16 male rats were used, half of them were sexually experienced while the other half were sexually inexperienced. After three sessions of sexual interaction to ejaculation, the sexually-experienced males presented shorter mount, intromission, and ejaculation latencies. Those rats presented a higher total dendritic density in the mPFC, and a higher numerical density of thin, mushroom, stubby, and wide spines. Sexual experience also increased the numerical density of mushroom spines in the NAcc. In both the mPFC and NAcc of the sexually experienced rats, there was a lower proportional density of thin spines and a higher proportional density of mushroom spines. Results show that the improvement in copulatory efficiency resulting from prior sexual experience in male rats is associated with changes in the proportional density of thin and mushroom dendritic spines in the mPFC and NAcc. This could represent the consolidation of afferent synaptic information in these brain regions, derived from the stimulus-sexual reward association.
Motor learning induces plastic changes in Purkinje cell dendritic spines in the rat cerebellum
2020, Neurologia
El lóbulo paramediano del cerebelo está involucrado en el desempeño correcto de las habilidades motoras a través de la práctica. Las espinas dendríticas son estructuras dinámicas que regulan la estimulación sináptica excitadora. En este trabajo se estudiaron los posibles cambios plásticos en espinas de células de Purkinje del lóbulo paramediano cerebelar de ratas, durante el aprendizaje motor.
Se entrenaron a ratas macho adultas durante un período de seis días, en un paradigma de aprendizaje motor acrobático y se cuantificó tanto la densidad como los tipos de espinas dendríticas en cada uno de los seis días de estudio, mediante una modificación al método de Golgi.
La curva de aprendizaje reflejó una disminución consistente de los errores cometidos en el transcurso de los días de entrenamiento. Así mismo, se observaron más espinas dendríticas en los días 2 y 6 y, en particular, más espinas delgadas en los días 1, 3 y 6, menos espinas en hongo el día 3, menos espinas gordas el día 1 y más espinas anchas los días 4 y 6.
El período inicial de aprendizaje motor podría estar asociado con el procesamiento rápido de la información sináptica subyacente y con un aparente «silenciamiento» de los procesos de consolidación mnémica, en una base de regulación de la excitabilidad neuronal.
The paramedian lobule of the cerebellum is involved in learning to correctly perform motor skills through practice. Dendritic spines are dynamic structures that regulate excitatory synaptic stimulation. We studied plastic changes occurring in the dendritic spines of Purkinje cells from the paramedian lobule of rats during motor learning.
Adult male rats were trained over a 6-day period using an acrobatic motor learning paradigm; the density and type of dendritic spines were determined every day during the study period using a modified version of the Golgi method.
The learning curve reflected a considerable decrease in the number of errors made by rats as the training period progressed. We observed more dendritic spines on days 2 and 6, particularly more thin spines on days 1, 3, and 6, fewer mushroom spines on day 3, fewer stubby spines on day 1, and more thick spines on days 4 and 6.
The initial stage of motor learning may be associated with fast processing of the underlying synaptic information combined with an apparent “silencing” of memory consolidation processes, based on the regulation of the neuronal excitability.
Biological intersection of sex, age, and environment in the corticotropin releasing factor (CRF) system and alcohol
2020, Neuropharmacology
The neuropeptide corticotropin-releasing factor (CRF) is critical in neural circuit function and behavior, particularly in the context of stress, anxiety, and addiction. Despite a wealth of preclinical evidence for the efficacy of CRF receptor 1 antagonists in reducing behavioral pathology associated with alcohol exposure, several clinical trials have had disappointing outcomes, possibly due to an underappreciation of the role of biological variables. Although he National Institutes of Health (NIH) now mandate the inclusion of sex as a biological variable in all clinical and preclinical research, the current state of knowledge in this area is based almost entirely on evidence from male subjects. Additionally, the influence of biological variables other than sex has received even less attention in the context of neuropeptide signaling. Age (particularly adolescent development) and housing conditions have been shown to affect CRF signaling and voluntary alcohol intake, and the interaction between these biological variables is particularly relevant to the role of the CRF system in the vulnerability or resilience to the development of alcohol use disorder (AUD). Going forward, it will be important to include careful consideration of biological variables in experimental design, reporting, and interpretation. As new research uncovers conditions in which sex, age, and environment play major roles in physiological and/or pathological processes, our understanding of the complex interaction between relevant biological variables and critical signaling pathways like the CRF system in the cellular and behavioral consequences of alcohol exposure will continue to expand ultimately improving the ability of preclinical research to translate to the clinic.
This article is part of the special issue on Neuropeptides.
Effects of prenatal binge-like ethanol exposure and maternal stress on postnatal morphological development of hippocampal neurons in rats
2017, International Journal of Developmental Neuroscience
Alcohol is one of the most commonly used drugs of abuse negatively affecting human health and it is known as a potent teratogen responsible for fetal alcohol syndrome (FAS), which is characterized by cognitive deficits especially pronounced in juveniles but ameliorating in adults. Searching for the potential morphological correlates of these effects, in this study, we compared the course of developmental changes in the morphology of principal hippocampal neurons in fetal-alcohol (A group), intubated control (IC group), and intact control male rats (C group) over a protracted period of the first two postnatal months.
Ethanol was administered to the pregnant Wistar dams intragastrically, throughout gestation days (GD) 7–20, at a total dose of 6 g/kg/day resulting in the mean blood alcohol concentration (BAC) of 246.6 ± 40.9 mg/dl. Ten morphometric parameters of Golgi-stained hippocampal neurons (pyramidal and granule) from CA1, CA3, and DG areas were examined at critical postnatal days (PD): at birth (PD1), at the end of the brain growth spurt period (PD10), in juveniles (PD30), and in young adults (PD60).
During postnatal development, the temporal pattern of morphometric changes was shown to be region-dependent with most significant alterations observed between PD1-30 in the CA region and between PD10-30 in the DG region. It was also parameter-dependent with the soma size (except for CA3 pyramids), number of primary dendrites, dendrite diameter, dendritic tortuosity and the branch angle demonstrating little changes, while the total dendritic field area, dendritic length, number of dendritic bifurcations, and spine density being highly increased in all hippocampal regions during the first postnatal month. Moderate ethanol intoxication and the maternal intubation stress during gestation, showed similar, transient effects on the neuron development manifested as a smaller soma size in granule cells, reduced dendritic parameters and lower spine density in pyramidal neurons at PD1. Full recovery from these effects took place within the first 10 postnatal days.
This study showed regional and temporal differences in the development of different morphometric features of principal hippocampal neurons in intact subjects over a protracted 2-months postnatal period. It also demonstrated an overlap in the effects of a moderate fetal ethanol intoxication and a mild maternal stress produced by the intragastric intubation, a commonly used method of ethanol administration to the pregnant dams. Fast recovery from the adverse effects on the soma size, dendritic arborization and spines density observed at birth indicates towards the fetal ethanol/stress induced developmental retardation.
The combined effects of developmental lead and ethanol exposure on hippocampus dependent spatial learning and memory in rats: Role of oxidative stress
2016, Food and Chemical Toxicology
Either developmental lead or ethanol exposure can impair learning and memory via induction of oxidative stress, which results in neuronal damage. we examined the effect of combined exposure with lead and ethanol on spatial learning and memory in offspring and oxidative stress in hippocampus. Rats were exposed to lead (0.2% in drinking water) or ethanol (4 g/kg) either individually or in combination in 5th day gestation through weaning. On postnatal days (PD) 30, rats were trained with six trials per day for 6 consecutive days in the water maze. On day 37, a probe test was done. Also, oxidative stress markers in the hippocampus were also evaluated. Results demonstrated that lead + ethanol co-exposed rats exhibited higher escape latency during training trials and reduced time spent in target quadrant, higher escape location latency and average proximity in probe trial test. There was significant decrease in superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GPx) activities and increase of malondialdehyde (MDA) levels in hippocampus of animals co-exposed to lead and ethanol compared with their individual exposures. We suggest that maternal consumption of ethanol during lead exposure has pronounced detrimental effects on memory, which may be mediated by oxidative stress.
Hippocampal hyperexcitability in fetal alcohol spectrum disorder: Pathological sharp waves and excitatory/inhibitory synaptic imbalance
2016, Experimental Neurology
Prenatal alcohol exposure (PAE) can lead to long-lasting neurological alterations that may predispose individuals to seizures and neurobehavioral dysfunction. To date, there exists limited information regarding the underlying pathophysiological mechanisms. The hippocampal CA3 region generates excitatory population activity, called sharp waves (SPWs), that provide an ideal model to study perturbations in neuronal excitability at the network and cellular levels. In the present study, we utilized a mouse model of PAE and used dual extracellular and whole-cell patch-clamp recordings from CA3 hippocampal pyramidal cells to evaluate the effect of 1st trimester-equivalent ethanol exposure (10% v/v) on SPW activity and excitatory/inhibitory balance. We observed that PAE significantly altered in vitro SPW waveforms, with an increased duration and amplitude, when compared to controls. In addition, PAE slices exhibited reduced pharmacological inhibition by the GABA-_A receptor antagonist bicuculline (BMI) on SPW activity, and increased population spike paired-pulse ratios, all indicative of network disinhibition within the PAE hippocampus. Evaluation of PAE CA3 pyramidal cell activity associated with SPWs, revealed increased action potential cell firing, which was accompanied by an imbalance of excitatory/inhibitory synaptic drive, shifted in favor of excitation. Moreover, we observed intrinsic changes in CA3 pyramidal activity in PAE animals, including increased burst firing and instantaneous firing rate. This is the first study to provide evidence for hippocampal dysfunction in the ability to maintain network homeostasis and underlying cellular hyperexcitability in a model of PAE. These circuit and cellular level alterations may contribute to the increased propensity for seizures and neurobehavioral dysfunction observed in patients with a history of PAE.

View all citing articles on Scopus

View full text

Prenatal and postnatal exposure to ethanol induces changes in the shape of the dendritic spines from hippocampal CA1 pyramidal neurons of the rat

Abstract

Alcohol

Toxicology

Physiol. Behav.

Exp. Neurol.

Dev. Brain Res.

Spine morphology of neurons in the avian forebrain is affected by rearing conditions

Behav. Neural. Biol.

A Golgi study of mouse hippocampal CA1 piramidal neurons followings perinatal ethanol exposure

Neurosci. Lett.