Prenatal Cocaine Exposure Decreases Parvalbumin-Immunoreactive Neurons and GABA-to-Projection Neuron Ratio in the Medial Prefrontal Cortex

McCarthy, Deirdre M.; Bhide, Pradeep G.

doi:10.1159/000337172

Cited by 24 publications

(22 citation statements)

References 89 publications

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“…Preclinical research has demonstrated significant effects of PCE on brain regions involved in emotional regulation, motivational control, and addiction vulnerability during adolescence (Chambers and Potenza, 2003)-eg, anterior cingulate (ACC) (Harvey, 2004), prefrontal cortex (PFC) (McCarthy and Bhide, 2012), and ventral striatum (VS) (Harvey et al, 2001;Wang et al, 2013). In humans, neurostructural (Rando et al, 2013) and neurofunctional (Li et al, 2009;Sheinkopf et al, 2009;Li et al, 2011) alterations (eg, during response inhibition, resting state alterations) in regions of the VS and PFC have also been reported among adolescents with PCE.…”

Section: Introductionmentioning

confidence: 99%

Prenatal Cocaine Exposure and Adolescent Neural Responses to Appetitive and Stressful Stimuli

Yip

Potenza

Balodis

et al. 2014

Neuropsychopharmacol

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Preclinical research has demonstrated the effects of prenatal cocaine exposure (PCE) on brain regions involved in emotional regulation, motivational control, and addiction vulnerability-eg, the ventral striatum (VS), anterior cingulate (ACC), and prefrontal cortex (PFC). However, little is known about the function of these regions in human adolescents with PCE. Twenty-two adolescents with PCE and 22 age-, gender-, and IQ-matched non-cocaine exposed (NCE) adolescents underwent functional magnetic resonance imaging (fMRI) during exposure to individually personalized neutral/relaxing, stressful, and favorite-food cues. fMRI data were compared using grouplevel two-tailed t-tests in the BioImage Suite. In comparison with NCE adolescents, PCE adolescents had reduced activity within cortical and subcortical brain regions, including the VS, ACC, and medial and dorslolateral PFC during exposure to favorite-food cues but did not differ in neural responses to stress cues. Subjective food craving was inversely related to dorsolateral PFC activation among PCE adolescents. Among PCE adolescents, subjective anxiety ratings correlated inversely with activations in the orbitofrontal cortex and brainstem during the stress condition and with ACC, dorsolateral PFC, and hippocampus activity during the neutral-relaxing condition. Thus adolescents with PCE display hypoactivation of brain regions involved in appetitive processing, with subjective intensities of craving and anxiety correlating inversely with extent of activation. These findings suggest possible mechanisms by which PCE might predispose to the development of addictions and related disorders, eg, substance-use disorders and binge-eating.

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Section: Introductionmentioning

confidence: 99%

Prenatal Cocaine Exposure and Adolescent Neural Responses to Appetitive and Stressful Stimuli

Yip

Potenza

Balodis

et al. 2014

Neuropsychopharmacol

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“…Prenatal phencyclidine (PCP) exposure reduces the density of PV-expressing cINs and disrupts the formation of prefrontal cortical circuits leading to behavioral deficits in mice 142 . Intriguingly, prenatal cocaine exposure, which is thought to primarily target dopaminergic and serotonergic systems, impairs tangential migration and causes a reduction of both the total number of cINs and the percentage of PV-expressing cINs in the medial prefrontal cortex of adult mice 143,144 . The epidemiological significance of in utero methamphetamine, PCP, and cocaine exposures, however, is unknown.…”

Section: Disruption Of Cortical Interneuron Developmentmentioning

confidence: 99%

Gene-environment interactions in cortical interneuron development and dysfunction: A review of preclinical studies

Ansen-Wilson

Lipinski

2017

NeuroToxicology

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Cortical interneurons (cINs) are a diverse group of locally projecting neurons essential to the organization and regulation of neural networks. Though they comprise only ~20% of neurons in the neocortex, their dynamic modulation of cortical activity is requisite for normal cognition and underlies multiple aspects of learning and memory. While displaying significant morphological, molecular, and electrophysiological variability, cINs collectively function to maintain the excitatory-inhibitory balance in the cortex by dampening hyperexcitability and synchronizing activity of projection neurons, primarily through use of the inhibitory neurotransmitter gamma-aminobutyric acid (GABA). Disruption of the excitatory-inhibitory balance is a common pathophysiological feature of multiple seizure and neuropsychiatric disorders, including epilepsy, schizophrenia, and autism. While most studies have focused on genetic disruption of cIN development in these conditions, emerging evidence indicates that cIN development is exquisitely sensitive to teratogenic disruption. Here, we review key aspects of cIN development, including specification, migration, and integration into neural circuits. Additionally, we examine the mechanisms by which prenatal exposure to common chemical and environmental agents disrupt these events in preclinical models. Understanding how genetic and environmental factors interact to disrupt cIN development and function has tremendous potential to advance prevention and treatment of prevalent seizure and neuropsychiatric illnesses.

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“…Previous preclinical and clinical studies have implicated PCE in impacting corticolimbic brain regions including the anterior cingulate (ACC) (Harvey, 2004), prefrontal cortex (PFC) (Grewen et al, 2014; McCarthy and Bhide, 2012; McCarthy et al, 2014), amygdala (Li et al, 2016) and ventral striatum (Harvey et al; Wang et al, 2013). Dysregulation of corticolimbic pathways have been shown in response to reward-related and stressful cues among individuals with obesity and with cocaine addiction (Jasinska et al, 2014; Jastreboff et al, 2013; Potenza, 2012).…”

Section: Introductionmentioning

confidence: 99%

“…Unlike some other functional connectivity analytic approaches, ICD is data-driven and does not require the definition of an arbitrary threshold or regions of interest and thus is model-free and unbiased. While ICD does not require hypotheses, given previous findings, we hypothesized that ICD would identify connectivity differences in corticolimbic (Harvey, 2004; McCarthy and Bhide, 2012; McCarthy et al, 2014) and DMN (Li et al, 2013; Li et al, 2011) regions during stressful and appetitive processing between the PCE and NDE groups, as well as reveal less well-characterized regions and networks. We also hypothesized that food-craving scores would be inversely correlated with the degree of connectivity in these regions during the stressful and appetitive conditions.…”

Section: Introductionmentioning

confidence: 99%

Altered functional connectivity to stressful stimuli in prenatally cocaine-exposed adolescents

Zakiniaeiz

Yip

Balodis

et al. 2017

Drug and Alcohol Dependence

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Background Prenatal cocaine exposure (PCE) is linked to addiction and obesity vulnerability. Neural responses to stressful and appetitive cues in adolescents with PCE versus those without have been differentially linked to substance-use initiation. However, no prior studies have assessed cue-reactivity responses among PCE adolescents using a connectivity-based approach. Methods Twenty-two PCE and 22 non-prenatally drug-exposed (NDE) age-, sex-, IQ- and BMI-matched adolescents participated in individualized guided imagery with appetitive (favorite-food), stressful and neutral-relaxing cue scripts during functional magnetic resonance imaging. Subjective favorite-food craving scores were collected before and after script exposure. A data-driven voxel-wise intrinsic connectivity distribution analysis was used to identify between-group differences and examine relationships with craving scores. Results A group-by-cue interaction effect identified a parietal lobe cluster where PCE versus NDE adolescents showed less connectivity during stressful and more connectivity during neutral-relaxing conditions. Follow-up seed-based connectivity analyses revealed that, among PCE adolescents, the parietal seed was positively connected to inferior parietal and sensory areas and negatively connected to corticolimbic during both stress and neutral-relaxing conditions. For NDE, greater parietal connectivity to parietal, cingulate and sensory areas and lesser parietal connectivity to medial prefrontal areas were found during stress compared to neutral-relaxing cueing. Craving scores inversely correlated with corticolimbic connectivity in PCE, but not NDE adolescents, during the favorite-food condition. Conclusions Findings from this first data-driven intrinsic connectivity analysis of PCE influences on adolescent brain function indicate differences relating to PCE status and craving. These findings provide insight into the developmental impact of in utero drug exposure.

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Prenatal Cocaine Exposure Decreases Parvalbumin-Immunoreactive Neurons and GABA-to-Projection Neuron Ratio in the Medial Prefrontal Cortex

Cited by 24 publications

References 89 publications

Prenatal Cocaine Exposure and Adolescent Neural Responses to Appetitive and Stressful Stimuli

Prenatal Cocaine Exposure and Adolescent Neural Responses to Appetitive and Stressful Stimuli

Gene-environment interactions in cortical interneuron development and dysfunction: A review of preclinical studies

Altered functional connectivity to stressful stimuli in prenatally cocaine-exposed adolescents

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