A rodent “self-report” measure of methamphetamine craving? Rat ultrasonic vocalizations during methamphetamine self-administration, extinction, and reinstatement

Mahler, Stephen V.; Moorman, David E.; Feltenstein, Matthew W.; Cox, Brittney M.; Ogburn, Katelyn B.; Bachar, Michal; McGonigal, Justin T.; Ghee, Shannon M.; See, Ronald E.

doi:10.1016/j.bbr.2012.08.023

Cited by 57 publications

(51 citation statements)

References 91 publications

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“…Considerable attention has been given to positive rewarding effects associated with MA addiction (Beckmann et al, 2010;Horton et al, 2011;Kamens et al, 2005;Mahler et al, 2013;Meyer et al, 2011;Mizoguchi et al, 2004;Shabani et al, 2011Shabani et al, , 2012aWheeler et al, 2009), whereas aversive effects that could limit intake have been given less consideration (Harrod et al, 2010;Pringle et al, 2008;Shabani et al, 2011Shabani et al, , 2012bWheeler et al, 2009). Greater Figure 3 (a) Methamphetamine (MA) consumption differs by Taar1 genotype.…”

Section: Discussionmentioning

confidence: 99%

Trace Amine-Associated Receptor 1 Regulation of Methamphetamine Intake and Related Traits

Harkness

Shi

Janowsky

et al. 2015

Neuropsychopharmacol

149

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Continued methamphetamine (MA) use is dependent on a positive MA experience and is likely attenuated by sensitivity to the aversive effects of MA. Bidirectional selective breeding of mice for high (MAHDR) or low (MALDR) voluntary consumption of MA demonstrates a genetic influence on MA intake. Quantitative trait locus (QTL) mapping identified a QTL on mouse chromosome 10 that accounts for greater than 50% of the genetically-determined differences in MA intake in the MAHDR and MALDR lines. The trace amine-associated receptor 1 gene (Taar1) is within the confidence interval of the QTL and encodes a receptor (TAAR1) that modulates monoamine neurotransmission and at which MA serves as an agonist. We demonstrate the existence of a non-functional allele of Taar1 in the DBA/2J mouse strain, one of the founder strains of the selected lines, and show that this non-functional allele co-segregates with high MA drinking and with reduced sensitivity to MA-induced conditioned taste aversion (CTA) and hypothermia. The functional Taar1 allele, derived from the other founder strain, C57BL/6J, segregates with low MA drinking and heightened sensitivity to MA-induced CTA and hypothermia. A role for TAAR1 in these phenotypes is corroborated in Taar1 transgenic mice: Taar1 knockout mice consume more MA and exhibit insensitivity to MA-induced CTA and hypothermia, compared with Taar1 wild-type mice. These are the first data to show that voluntary MA consumption is, in part, regulated by TAAR1 function. Behavioral and physiological studies indicate that TAAR1 function increases sensitivity to aversive effects of MA, and may thereby protect against MA use.

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Section: Discussionmentioning

confidence: 99%

Trace Amine-Associated Receptor 1 Regulation of Methamphetamine Intake and Related Traits

Harkness

Shi

Janowsky

et al. 2015

Neuropsychopharmacol

149

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“…Consistent with this hypothesis, in dependent rats but not nondependent rats, we observed that a subset of rats that displayed high alcoholin take also had higher levels of anticipatory 50 kHz USVs compared with low-alcohol-intake rats. Previous studies have reported an increase in 50 kHz USVs in response to cues paired with appetitive stimuli, such as food [8,9], copulation [10,11], and cocaine [11,12]. Rats that had extinguished methamphetamine self-administration and then given a methamphetamine priming injection or exposed to drug-paired cues robustly emitted 50 kHz USVs and rein-stated drug-seeking behavior [12].…”

Section: Discussionmentioning

confidence: 99%

“…Previous studies have reported an increase in 50 kHz USVs in response to cues paired with appetitive stimuli, such as food [8,9], copulation [10,11], and cocaine [11,12]. Rats that had extinguished methamphetamine self-administration and then given a methamphetamine priming injection or exposed to drug-paired cues robustly emitted 50 kHz USVs and rein-stated drug-seeking behavior [12]. If these cue-induced USVs are thought to reflect an increased appetitive or motivational state, it may suggest that a subgroup of alcohol-dependent rats (i.e., the high drinkers) in the present study demonstrated an increase in motivational salience (i.e., an increase in alcohol-seeking behavior/craving/incentive salience), reflected by higher anticipatory50 kHz USVs.…”

Section: Discussionmentioning

confidence: 99%

“…Previous reports have shown that 50 kHz USVs are elicited by cues that predict rewarding stimuli, such as food [8,9], copulation [10], cocaine [11], and rewarding brain stimulation [8]. Thus, 50 kHz USVs may be an index of motivation during reward anticipation [1,11,12]. Most studies that have investigated the relationship between 50 kHz USVs and drugs of abuse have focused on psychostimulants; few studies have examined 50 kHz USVs in relation to alcohol self-administration.…”

Section: Introductionmentioning

confidence: 99%

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Anticipatory 50kHz ultrasonic vocalizations are associated with escalated alcohol intake in dependent rats

Buck¹,

Malavar²,

George³

et al. 2014

Behavioural Brain Research

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Rats emit 50 kHz ultrasonic vocalizations (USVs) in situations of increased motivation, such as during the anticipation of palatable food or drugs of abuse. Whether the same holds true for the anticipation of alcohol intake remains unknown. Alcohol drinking in a nondependent state is thought to be mediated by its rewarding effects (positive reinforcement), whereas drinking in the dependent state is motivated by alcohol’s stress-relieving effects (negative reinforcement). Here, we measured context-elicited 50 kHz USVs in alcohol-dependent (alcohol vapor-exposed) and nondependent rats immediately before operant alcohol self-administration sessions. Dependent rats showed escalated levels of alcohol intake compared with nondependent rats. Overall, dependent and nondependent rats showed similar levels of anticipatory 50 kHz USVs. However, the number of anticipatory USVs was positively correlated with alcohol intake in dependent rats but not nondependent rats. Additionally, dependent rats with higher alcohol intake displayed increased anticipatory 50 kHz USVs compared with rats that had lower alcohol intake, whereas no difference was observed between rats with high and low alcohol intake in the nondependent group. Increased 50 kHz USVs were specific for the anticipation of alcohol self-administration and did not generalize to a novel environment. These findings suggest that anticipatory 50 kHz USVs may be an indicator of context-elicited negative reinforcement learning.

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“…In particular, USVs in the upper frequency range near 50 kHz predominate in positive contexts including mating, exploration, play, and also in the anticipation of rewards such as food and electrical stimulation (Bialy et al 2000; Burgdorf et al 2006; Knutson et al 1998; 1999). As a result, 50 kHz USVs have been proposed to be an index of affective state and further, as a preclinical analogue to human “self-report” of subjective states (Mahler et al 2013; Panksepp et al 2002). Given the potential motivational significance of these USVs, it is possible that they index an aspect of drug sensitivity distinct from locomotion, and may thus distinguish sign- and goal-trackers, especially after administration of addictive drugs.…”

Section: Introductionmentioning

confidence: 99%

Individual differences in food cue responsivity are associated with acute and repeated cocaine-induced vocalizations, but not cue-induced vocalizations

2016

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Rationale Individuals prone to attribute incentive salience to food-associated stimuli (“cues”) are also more sensitive to cues during drug-seeking and drug-taking. This may be due in part to a difference in sensitivity to the affective or other stimulus properties of the drug. In rats, these properties are associated with 50 kHz ultrasonic vocalizations (USVs), in that they are elicited during putative positive affective and motivational states, including in response to drugs of abuse. Objectives We sought to determine whether individual differences in the tendency to attribute incentive salience to a food cue (as measured by approach) were associated with differences in cocaine-induced USVs. We also tested whether the food cue would elicit USVs, and if this response was related to approach to the food cue. Methods In experiment 1, rats underwent Pavlovian Conditioned Approach (PavCA) training where they learned to associate a cue (an illuminated lever) with the delivery of a food pellet into a food cup. Subjects were categorized based on their approach to the cue (“sign-trackers”), or to the food cup (“goal-trackers”). Rats subsequently underwent nine testing days in which they were given saline or cocaine (10 mg/kg i.p), and placed into a locomotor chamber. In experiment 2, rats were first tested in the locomotor chambers for one saline-treated day followed by one cocaine-treated day, and then trained in PavCA. USVs were recorded from a subset of individuals during the last day of PavCA to determine if the food cue would elicit USVs. Results Sign-trackers produced 5 - 24 times more cocaine-induced 50 kHz USVs compared to goal-trackers for all days of experiment 1, and this response sensitized with repeated cocaine, only in sign-trackers. Similarly in experiment 2, individuals that produced the most cocaine-induced USVs on a single exposure also showed the greatest tendency to sign-track during PavCA. Lastly, while sign-trackers produced more USVs during PavCA generally, the cue itself did not elicit additional USVs in sign- or goal-trackers. Conclusions These results indicate a robust and consistent relationship between approach to a food cue and cocaine-induced USV production. Thus, these USVs may index the neurobiological differences underlying the behavioral distinctions of sign- and goal-trackers.

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A rodent “self-report” measure of methamphetamine craving? Rat ultrasonic vocalizations during methamphetamine self-administration, extinction, and reinstatement

Cited by 57 publications

References 91 publications

Trace Amine-Associated Receptor 1 Regulation of Methamphetamine Intake and Related Traits

Trace Amine-Associated Receptor 1 Regulation of Methamphetamine Intake and Related Traits

Anticipatory 50kHz ultrasonic vocalizations are associated with escalated alcohol intake in dependent rats

Individual differences in food cue responsivity are associated with acute and repeated cocaine-induced vocalizations, but not cue-induced vocalizations

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