Ontogenesis of behavioral sensitization and conditioned place preference induced by psychostimulants in laboratory rodents

Tirelli, Ezio; Laviola, Giovanni; Adriani, Walter

doi:10.1016/s0149-7634(03)00018-6

Cited by 312 publications

(233 citation statements)

References 118 publications

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“…Comparatively, adolescents (P44) formed a strong preference for a context paired with the lowest (10 mg/kg) dose of cocaine used, corroborating findings from Schramm-Sapyta et al (2006). This is consistent with the notion that adolescence is characterized by a high sensitivity to reward (Chambers et al, 2003;Tirelli et al, 2003;Ernst et al, 2006), although this sensitivity may partly be caused by enhanced cortical drive as suggested here. Adolescents also maintain context-drug associations 75% longer than adults during extinction of cocaineconditioned place preferences and demonstrate stronger drug-primed reinstatement (Brenhouse and Andersen, 2008).…”

Section: Discussionsupporting

confidence: 87%

“…The assessment of motivational responsiveness to stimulants during development is not well defined in the literature for a number of reasons. Inconsistencies in paradigms used, handling stressors, ages, sex (Campbell et al, 2000), drug doses, and the use of stimulants with different behavioral sequelae, such as stereotypy, yield variable conclusions, ranging from decreased amphetamine place conditioning to a heightened sensitivity to cocaine place conditioning in adolescence (Campbell et al, 2000;Tirelli et al, 2003;Badanich et al, 2006;Balda et al, 2006;Schramm-Sapyta et al, 2006) (for review, see Brenhouse and Andersen, 2008). For example, handling is one such variable to consider.…”

Section: Discussionmentioning

confidence: 99%

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Transient D₁Dopamine Receptor Expression on Prefrontal Cortex Projection Neurons: Relationship to Enhanced Motivational Salience of Drug Cues in Adolescence

Brenhouse¹,

Sonntag²,

Andersen³

2008

J. Neurosci.

266

292

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Adolescence is a transitional period during development that is associated with a greater likelihood of addiction to drugs than any other age. In the prefrontal cortex (PFC), D 1 dopamine receptors mediate motivational salience attribution, which plays a role in addiction. Here, we investigated the relationship of age-related D 1 dopamine receptor expression in the PFC with the maturation of cocaine place conditioning. Confocal microscopy revealed that retrogradely traced cortical output neurons to the nucleus accumbens express higher levels of D 1 receptors during adolescence compared with younger and older ages. D 1 expression does not change on GABAergic interneurons across age. Adolescent differences in D 1 expression occur independently of cortical-accumbens connectivity, which proliferates through adulthood. Behaviorally, adolescent rats are more sensitive to cocaine place conditioning than younger and older rats. However, microinjections of the D 1 antagonist SCH23390 into the PFC blocked adolescent place preferences, whereas microinjections of D 1 agonists dose-dependently increased preferences for cocaine-associated environments previously not preferred by juveniles. These results suggest that the heightened expression of D 1 receptors on cortical-accumbens projections may help explain increased sensitivity to environmental events and addictive behaviors during adolescence, whereas the paucity of D 1 -expressing projections may reduce risk in juveniles.

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Section: Discussionsupporting

confidence: 87%

Section: Discussionmentioning

confidence: 99%

Transient D₁Dopamine Receptor Expression on Prefrontal Cortex Projection Neurons: Relationship to Enhanced Motivational Salience of Drug Cues in Adolescence

Brenhouse¹,

Sonntag²,

Andersen³

2008

J. Neurosci.

266

292

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“…As in our previous work, in this study, we define 'early adolescence' in C57BL/6 mice as the period between the day of weaning and PND 32. These definitions seem now to be a consensus in the mouse literature (eg, (Spear, 2000;Laviola et al, 2003;Schneider, 2013;Tirelli et al, 2003). This is not an absolute margin, but rather an age range during which mice exhibit distinct neurobehavioral characteristics.…”

Section: Experimental Procedures and Timelinementioning

confidence: 99%

Amphetamine in Adolescence Disrupts the Development of Medial Prefrontal Cortex Dopamine Connectivity in a dcc-Dependent Manner

Reynolds

Makowski

Yogendran

et al. 2014

Neuropsychopharmacol

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Initiation of drug use during adolescence is a strong predictor of both the incidence and severity of addiction throughout the lifetime. Intriguingly, adolescence is a period of dynamic refinement in the organization of neuronal connectivity, in particular medial prefrontal cortex (mPFC) dopamine circuitry. The guidance cue receptor, DCC (deleted in colorectal cancer), is highly expressed by dopamine neurons and orchestrates their innervation to the mPFC during adolescence. Furthermore, we have shown that amphetamine in adolescence regulates DCC expression in dopamine neurons. Drugs in adolescence may therefore induce their enduring behavioral effects via DCC-mediated disruption in mPFC dopamine development. In this study, we investigated the impact of repeated exposure to amphetamine during adolescence on both the development of mPFC dopamine connectivity and on salience attribution to drug context in adulthood. We compare these effects to those induced by adult exposure to an identical amphetamine regimen. Finally, we determine whether DCC signaling within dopamine neurons is necessary for these events. Exposure to amphetamine in adolescence, but not in adulthood, leads to an increase in the span of dopamine innervation to the mPFC, but a reduction of presynaptic sites present on these axons. Amphetamine treatment in adolescence, but not in adulthood, also produces an increase in salience attribution to a previously drug-paired context in adulthood. Remarkably, DCC signaling within dopamine neurons is required for both of these effects. Drugs of abuse in adolescence may therefore induce their detrimental behavioral consequences by disrupting mesocortical dopamine development through alterations in the DCC signaling cascade.

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“…Conversely, adolescent but not adult mice exhibited greater motor activity to a challenge dose of AMPH (2.0 mg/kg), after a history of exposure to 10.0 mg/kg AMPH (Adriani et al., 1998). It has been suggested that the mechanisms responsible for the expression of long‐term sensitization to psychostimulants are just concluding maturation by the fourth week of rats’ postnatal life (Tirelli, Laviola, & Adriani, 2003), which could explain the variability in the reported results.…”

Section: Discussionmentioning

confidence: 96%

Amphetamine, but not methylphenidate, increases ethanol intake in adolescent male, but not in female, rats

et al. 2018

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IntroductionThere has been an increasing interest in analyzing the interactions between stimulants and ethanol during childhood and adolescence. Stimulants are used to treat attention‐deficit hyperactivity disorder (ADHD) in these developmental stages, during which ethanol initiation and escalation often occur.MethodsThis study assessed the effects of repeated d‐amphetamine (AMPH) or methylphenidate (MPH) treatment during adolescence [male and female Wistar rats, between postnatal day (PD) 28 to PD34, approximately] on the initiation of ethanol intake during a later section of adolescence (PD35 to PD40).ResultsAmphetamine and MPH exerted reliable acute motor stimulant effects, but there was no indication of sensitized motor or anxiety responses. MPH did not affect dopamine (DA) levels, whereas AMPH significantly reduced insular levels of DA in both sexes and norepinephrine levels in females only. Repeated treatment with AMPH, but not with MPH, enhanced ethanol intake during late adolescence in male, but not in female, rats.ConclusionA short treatment with AMPH during adolescence significantly altered DA levels in the insula, both in male and females, and significantly enhanced ethanol intake in males. The present results suggest that, in adolescent males, a very brief history of AMPH exposure can facilitate the initiation of ethanol intake.

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Ontogenesis of behavioral sensitization and conditioned place preference induced by psychostimulants in laboratory rodents

Cited by 312 publications

References 118 publications

Transient D₁Dopamine Receptor Expression on Prefrontal Cortex Projection Neurons: Relationship to Enhanced Motivational Salience of Drug Cues in Adolescence

Transient D₁Dopamine Receptor Expression on Prefrontal Cortex Projection Neurons: Relationship to Enhanced Motivational Salience of Drug Cues in Adolescence

Amphetamine in Adolescence Disrupts the Development of Medial Prefrontal Cortex Dopamine Connectivity in a dcc-Dependent Manner

Amphetamine, but not methylphenidate, increases ethanol intake in adolescent male, but not in female, rats

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Ontogenesis of behavioral sensitization and conditioned place preference induced by psychostimulants in laboratory rodents

Cited by 312 publications

References 118 publications

Transient D1Dopamine Receptor Expression on Prefrontal Cortex Projection Neurons: Relationship to Enhanced Motivational Salience of Drug Cues in Adolescence

Transient D1Dopamine Receptor Expression on Prefrontal Cortex Projection Neurons: Relationship to Enhanced Motivational Salience of Drug Cues in Adolescence

Amphetamine in Adolescence Disrupts the Development of Medial Prefrontal Cortex Dopamine Connectivity in a dcc-Dependent Manner

Amphetamine, but not methylphenidate, increases ethanol intake in adolescent male, but not in female, rats

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Transient D₁Dopamine Receptor Expression on Prefrontal Cortex Projection Neurons: Relationship to Enhanced Motivational Salience of Drug Cues in Adolescence

Transient D₁Dopamine Receptor Expression on Prefrontal Cortex Projection Neurons: Relationship to Enhanced Motivational Salience of Drug Cues in Adolescence