Individual differences in anticipatory activity to food rewards predict cue-induced appetitive 50-kHz calls in rats

Brenes, Juan C.; Schwarting, Rainer K.W.

doi:10.1016/j.physbeh.2015.05.012

Cited by 32 publications

(25 citation statements)

References 66 publications

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“…This USV response habituated in both groups over time, perhaps indicating a decreasing appetitive state separable from the approach behaviors observed throughout the session. Additionally, explanation for our low rate of cue-induced USVs from either group may be a result of several factors, including predictability of the cue presentations, (Burgdorf et al 2000; Burgdorf et al 2005), food deprivation (Brenes and Schwarting 2014; Knutson et al 2002), the nature of the CS (auditory vs visual) (Brenes and Schwarting 2015; Meyer et al 2014), or the form of the approach measured (Brenes and Schwarting 2015). Thus, whether or not a cue elicits the initiation and/or enhancement in USVs is dependent on the specifics of the paradigm, rather than being a consistent response to a broad class of reward-associated stimuli.…”

Section: Discussionmentioning

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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Section: Discussionmentioning

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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“…Considering that laboratory rodents prefer larger and complex cages, social contact, and exercise (Olsson and Dahlborn, 2002;Van Loo et al, 2003;Heyse et al, 2015), we assume that EE is rewarding for rodents. Rats emit high-frequency (e.g., 50-kHz) USVs in social (e.g., mating and rough-and-tumble play) and non-social rewarding situations (e.g., brain stimulation of reward centers and administration of psychostimulants) (Burgdorf et al, 2000;Williams and Undieh, 2010;Pereira et al, 2014;Brenes and Schwarting, 2015). Out of the different 50-kHz calls, the FM subtypes (e.g., step-flats, step-trills, and trills) are indicative of a high, positive affective state (Burgdorf et al, 2007;Burgdorf et al, 2008;Burgdorf et al, 2011).…”

Section: Methodsmentioning

confidence: 99%

“…For instance, the between-group differences in the number of 50-kHz calls were 2.28 and 3.67-fold higher in the REE group, with the lowest call rate of the REE rats being even higher than the highest point of the CEE rats. Considering that 50-kHz calls may signal a state of appetitive incentive motivation (Brenes and Schwarting, 2014;Brenes and Schwarting, 2015), the differences in USVs suggest that unpredictable and restricted access to the EE cage could have extended and enhanced the rewarding properties of the EE stimuli. In support to the latter, we have previously found that rats trained to run a runway to enter a locked running wheel, displayed almost the same latencies and rates of 50-kHz calls than those with the unlocked wheel, suggesting that the structural features of the wheels were equally attractive for both groups (Heyse et al, 2015).…”

Section: Methodsmentioning

confidence: 99%

“…USVs emitted within a frequency range of 19-32 kHz were considered as 22-kHz USVs, and USVs between 33 and 96 kHz were defined as 50-kHz USVs (Brenes et al, 2016). Later, experienced observers manually filtered and selected the genuine USVs based on our own criteria reported elsewhere (Brenes and Schwarting, 2015;Brenes et al, 2016). Briefly, if two 50-kHz elements were at least .048 s apart, two independent 50-kHz calls were counted.…”

Section: Analysis Of Usvsmentioning

confidence: 99%

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Neurobehavioral Effects of Restricted and Unpredictable Environmental Enrichment in Rats

2020

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To study how motivational factors modulate experience-dependent neurobehavioral plasticity, we modify a protocol of environmental enrichment (EE) in rats. We assumed that the benefits derived from EE might vary according to the level of incentive salience attributed to it. To enhance the rewarding properties of EE, access to the EE cage varied randomly from 2 to 48 h for 30 days (REE). The REE group was enriched only 50% of the time and was compared to standard housing and continuous EE (CEE) groups. As behavioral readout, we analyzed the spontaneous activity and the ultrasonic vocalizations (USVs) within the EE cage weekly, and in the open field test at the end of the experiment. In the cage, REE increased the utilization of materials, physical activity, and the rate of appetitive USVs. In the OF, the CEE-induced enhancements in novelty habituation and social signaling were equaled by the REE. At the neural level, we measured the expression of genes related to neural plasticity and epigenetic regulations in different brain regions. In the dorsal striatum and hippocampus, REE upregulated the expression of the brainderived neurotrophic factor, its tropomyosin kinase B receptor, and the DNA methyltransferase 3A. Altogether, our results suggest that the higher activity within the cage and the augmented incentive motivation provoked by the REE boosted its neurobehavioral effects equaling or surpassing those observed in the CEE condition. As constant exposures to treatments or stimulating environments are virtually impossible for humans, restricted EE protocols would have greater translational value than traditional ones.

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“…Indeed, increased anticipatory motor behavior was positively correlated with frequency of high ultrasonic vocalizations (Brenes and Schwarting, 2015). High ultrasonic vocalizations were emitted in anticipation of several rewarding stimuli, including food (Buck et al , 2014b; Opiol et al , 2015), a cocaine or ethanol reward (Buck et al , 2014a; Ma et al , 2010), and being reunited with a cage mate after a period of social isolation (Willey and Spear, 2012).…”

Section: Translational Assessments Of Reward and Motivationmentioning

confidence: 99%

Translational Assessment of Reward and Motivational Deficits in Psychiatric Disorders

Der-Avakian

Barnes

Markou

et al. 2015

Translational Neuropsychopharmacology

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Deficits in reward and motivation are common symptoms characterizing several psychiatric and neurological disorders. Such deficits may include anhedonia, defined as loss of pleasure, as well as impairments in anticipatory pleasure, reward valuation, motivation/effort, and reward learning. This chapter describes recent advances in the development of behavioral tasks used to assess different aspects of reward processing in both humans and non-human animals. While earlier tasks were generally developed independently with limited cross-species correspondence, a newer generation of translational tasks has emerged that are theoretically and procedurally analogous across species and allow parallel testing, data analyses, and interpretation between human and rodent behaviors. Such enhanced conformity between cross-species tasks will facilitate investigation of the neurobiological mechanisms underlying discrete reward and motivated behaviors and is expected to improve our understanding and treatment of neuropsychiatric disorders characterized by reward and motivation deficits.

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Individual differences in anticipatory activity to food rewards predict cue-induced appetitive 50-kHz calls in rats

Cited by 32 publications

References 66 publications

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

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

Neurobehavioral Effects of Restricted and Unpredictable Environmental Enrichment in Rats

Translational Assessment of Reward and Motivational Deficits in Psychiatric Disorders

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