Exercise reward induces appetitive 50-kHz calls in rats

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

doi:10.1016/j.physbeh.2015.04.021

Cited by 19 publications

(16 citation statements)

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“…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). Once the rats with the unlocked wheel exercised, the rate of 50-kHz calls increased substantially, indicating that the activity on its own was also rewarding for them (Heyse et al, 2015).…”

Section: Methodsmentioning

confidence: 55%

“…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). Once the rats with the unlocked wheel exercised, the rate of 50-kHz calls increased substantially, indicating that the activity on its own was also rewarding for them (Heyse et al, 2015). As the REE rats were housed in groups of five during the non-EE period, entering the EE cage offered the opportunity for interacting with non-cagemates rats, which could have also been a great source of reward.…”

Section: Methodsmentioning

confidence: 55%

“…REE Increases the Activity and the Rate of Appetitive USVs in the Cage Several lines of evidence have shown that restricted or unpredictable access to rewarding stimuli (e.g., food or drugs of abuse) increases both incentive motivation attributed to reward-predicting cues and approaching and consummatory responses toward the reward (Anselme et al, 2013;Brenes and Schwarting, 2014;Schultz, 2016;Kreisler et al, 2018). 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).…”

Section: Methodsmentioning

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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Section: Methodsmentioning

confidence: 55%

Section: Methodsmentioning

confidence: 55%

Section: Methodsmentioning

confidence: 99%

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Neurobehavioral Effects of Restricted and Unpredictable Environmental Enrichment in Rats

2020

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“…High-frequency calls are produced by juvenile or adult rats during rough-and-tumble play [41], during mating [41][42][43][44], as an expression of reward during voluntary exercise [45], as well as in response to drugs of abuse [46,47], and it is widely accepted today that they reflect a positive affective state [46,48,49]. Consequently, one of their functions appears to be the communication of emotional states to conspecifics [50].…”

Section: Introductionmentioning

confidence: 99%

Reduction in 50-kHz call-numbers and suppression of tickling-associated positive affective behaviour after lesioning of the lateral hypothalamic parvafox nucleus in rats

Roccaro-Waldmeyer

Babalian

Müller

et al. 2016

Behavioural Brain Research

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h i g h l i g h t s• Wistar rats were tickled before and after excitotoxic lesioning of the lateral hypothalamic parvafox nucleus.• Ultrasonic vocalisations (USVs) that were emitted during the tickling of rats and their tendency to approach and follow the experimenter's hand were analysed.• Lesioning was considered successful if the number of parvalbuminimmunoreactive (PV-ir) cells in the area of the parvafox nucleus was reduced beyond a threshold level.• Rats with bilaterally successful lesions manifested the most profound surgery-associated reduction in the number of 50-kHz USVs and in the tendency to approach and follow the experimenter's hand.• Positive correlations were found between each of the four investigated parameters. g r a p h i c a l a b s t r a c tThe parvafox nucleus is located ventrolaterally in the lateral hypothalamic area (LHA). Its core and shell are composed of neurons expressing the calcium-binding protein parvalbumin (PV) and the transcription factor Foxb1, respectively. Given the known functions of the LHA and that the parvafox nucleus receives afferents from the lateral orbitofrontal cortex and projects to the periaqueductal gray matter, a functional role of this entity in the expression of positive emotions has been postulated.The purpose of the present study was to ascertain whether the deletion of neurons in the parvafox nucleus influenced the tickling-induced 50-kHz calls, which are thought to reflect positive affective states, in rats. To this end, tickling of the animals (heterospecific play) was combined with intracerebral injections of the excitotoxin kainic acid into the parvafox nucleus.The most pronounced surgery-associated reduction in 50-kHz call-numbers was observed in the group of rats in which, on the basis of PV-immunoreactive-cell counts in the parvafox nucleus, bilateral lesions had been successfully produced. Two other parameters that were implemented to quantify positive affective behaviour, namely, an approach towards and a following of the hand of the tickling * Corresponding author at: Institute of Anatomy, University of Fribourg, Rte A. Gockel 1, CH-1700 Fribourg, Switzerland.E-mail address: marco.celio@unifr.ch (M.R. Celio). 1Published in which should be cited to refer to this work.http://doc.rero.ch experimenter, were likewise most markedly suppressed in the group of rats with bilaterally successful lesions. Furthermore, positive correlations were found between each of the investigated parameters. Our data afford evidence that the parvafox nucleus plays a role in the production of 50-kHz calls in rats, and, more generally, in the expression of positive emotions.

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“…Indeed, our use of the term anticipatory can be 306 questioned, given the findings. Heyse et al (2015) found that rats would emit 50 kHz calls in 307 anticipation of access to a running wheel. Others have found that individual rats vocalize more in a 308 chamber associated with play than in a habituated control chamber (Knutson et al, 1998) The second hypothesis was that more USVs would be emitted by the tickled than by control rats 322 when exposed to the conditioned odour following exposure to an aversive odour.…”

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Odour conditioning of positive affective states: Rats can learn to associate an odour with being tickled

Bombail

Jerome

Lam

et al. 2019

Preprint

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Most associative learning tests in rodents use negative stimuli, such as an electric shock. We investigated if young rats can learn to associate the presence of an odour with the experience of being tickled (i.e. using an experimenter’s hand to mimic rough-and-tumble play), shown to elicit 50 kHz ultrasonic vocalisations (USVs), which are indicative of positive affect. Male, pair-housed Wistar rats (N=24) were all exposed to two neutral odours (A and B) presented in a perforated container on alternate days in a test arena. Following 60s of exposure, the rats were either tickled on days when odour A (n=8) or odour B (n=8) was present, or never tickled (n=8). When tickled, rats produced significantly more 50 kHz USVs compared to the days when not being tickled, and compared to control rats. The level of anticipatory 50 kHz USVs in the 60s prior to tickling did not differ significantly between the tickled and control rats. Following the odour conditioning, rats were exposed successively in the same arena to three odours: an unknown neutral odour, extract of fox faeces, and either odours A or B. Compared to controls, 50 kHz USVs of tickled rats increased when exposed to the odour they had previously experienced when tickled, indicating that these rats had learned to associate the odour with the positive experience of being tickled. In a test with free access for 5 min to both arms of a T-maze, each containing one of the odours, rats tickled with odour A spent more time in the arm with this odour. This work is the first to test in a fully balanced design whether odours can be conditioned to tickling, and indicates that positive odour conditioning has potential to be used as an alternative to negative conditioning tests.

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Exercise reward induces appetitive 50-kHz calls in rats

Cited by 19 publications

References 88 publications

Neurobehavioral Effects of Restricted and Unpredictable Environmental Enrichment in Rats

Neurobehavioral Effects of Restricted and Unpredictable Environmental Enrichment in Rats

Reduction in 50-kHz call-numbers and suppression of tickling-associated positive affective behaviour after lesioning of the lateral hypothalamic parvafox nucleus in rats

Odour conditioning of positive affective states: Rats can learn to associate an odour with being tickled

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