Dissimilar interaction between dopaminergic and cholinergic systems in the initiation of emission of 50-kHz and 22-kHz vocalizations

Silkstone, Michael; Brudzyński, Stefan M.

doi:10.1016/j.pbb.2019.172815

Cited by 17 publications

(13 citation statements)

References 96 publications

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“…Although the association between acetylcholinesterase activity with USVs during fear extinction was not investigated, the induction of 22 kHz USVs involves activation of the ascending cholinergic afferents from the mesolimbic cholinergic system ( Brudzynski and Bihari, 1990 ; Brudzynski et al, 1991 ; Brudzynski, 2001 , 2007 , 2021 ; Machold, 2013 ). Emission of 50 kHz USVs is regulated by dopaminergic mechanisms, however, studies suggest that emotional regulation of both 22 and 50 kHz USVs may be due to the interaction between dopaminergic and cholinergic mechanisms (see Silkstone and Brudzynski, 2020 ; Brudzynski, 2021 ). The potential role of individual differences in cholinergic and dopaminergic systems in mediating the divergence in freezing or USVs between ER and EC phenotypes, and/or potential sex differences in USVs during fear conditioning remain to be investigated.…”

Section: Discussionmentioning

confidence: 99%

Individual Differences in Conditioned Fear and Extinction in Female Rats

Tryon

Kellis

Kaigler

et al. 2021

Front. Behav. Neurosci.

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The inability to extinguish a traumatic memory is a key aspect of post-traumatic stress disorder (PTSD). While PTSD affects 10–20% of individuals who experience a trauma, women are particularly susceptible to developing the disorder. Despite this notable female vulnerability, few studies have investigated this particular resistance to fear extinction observed in females. Similar to humans, rodent models of Pavlovian fear learning and extinction show a wide range of individual differences in fear learning and extinction, although female rodents are considerably understudied. Therefore, the present study examined individual differences in fear responses, including freezing behavior and ultrasonic vocalizations (USVs), of female Long–Evans rats during acquisition of fear conditioning and cued fear extinction. Similar to prior studies in males, female rats displayed individual variation in freezing during cued fear extinction and were divided into extinction competent (EC) and extinction resistant (ER) phenotypes. Differences in freezing between ER and EC females were accompanied by shifts in rearing during extinction, but no darting was seen in any trial. Freezing behavior during fear learning did not differ between the EC and ER females. Vocalizations emitted in the 22 and 50 kHz ranges during fear learning and extinction were also examined. Unlike vocalizations seen in previous studies in males, very few 22 kHz distress vocalizations were emitted by female rats during fear acquisition and extinction, with no difference between ER and EC groups. Interestingly, all female rats produced significant levels of 50 kHz USVs, and EC females emitted significantly more 50 kHz USVs than ER rats. This difference in 50 kHz USVs was most apparent during initial exposure to the testing environment. These results suggest that like males, female rodents show individual differences in both freezing and USVs during fear extinction, although females appear to vocalize more in the 50 kHz range, especially during initial periods of exposure to the testing environment, and emit very few of the 22 kHz distress calls that are typically observed in males during fear learning or extinction paradigms. Overall, these findings show that female rodents display fear behavior repertoires divergent from males.

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Section: Discussionmentioning

confidence: 99%

Individual Differences in Conditioned Fear and Extinction in Female Rats

Tryon

Kellis

Kaigler

et al. 2021

Front. Behav. Neurosci.

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“…Pharmacological antagonism of the mesolimbic dopaminergic system did not automatically increase the emission of 22 kHz vocalizations. On the other hand, cholinergic overstimulation of the aversive system with abundant emission of 22 kHz vocalizations caused a delayed rebound effect in the form of the spontaneous generation of 50 kHz calls in a proportional way to the intensity of the initial aversive response [ 260 ]. Moreover, the rebound emission of 50 kHz vocalizations was entirely blocked by haloperidol, proving that the emission of 50 kHz from whatever reason is generated by dopamine [ 260 ].…”

Section: Vocalization As Expression Of Emotional Arousalmentioning

confidence: 99%

Biological Functions of Rat Ultrasonic Vocalizations, Arousal Mechanisms, and Call Initiation

Brudzyński

2021

Brain Sciences

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This review summarizes all reported and suspected functions of ultrasonic vocalizations in infant and adult rats. The review leads to the conclusion that all types of ultrasonic vocalizations subserving all functions are vocal expressions of emotional arousal initiated by the activity of the reticular core of the brainstem. The emotional arousal is dichotomic in nature and is initiated by two opposite-in-function ascending reticular systems that are separate from the cognitive reticular activating system. The mesolimbic cholinergic system initiates the aversive state of anxiety with concomitant emission of 22 kHz calls, while the mesolimbic dopaminergic system initiates the appetitive state of hedonia with concomitant emission of 50 kHz vocalizations. These two mutually exclusive arousal systems prepare the animal for two different behavioral outcomes. The transition from broadband infant isolation calls to the well-structured adult types of vocalizations is explained, and the social importance of adult rat vocal communication is emphasized. The association of 22 kHz and 50 kHz vocalizations with aversive and appetitive states, respectively, was utilized in numerous quantitatively measured preclinical models of physiological, psychological, neurological, neuropsychiatric, and neurodevelopmental investigations. The present review should help in understanding and the interpretation of these models in biomedical research.

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“…Alternatively, we may speculate that rats that emitted mostly 22-kHz USVs in response to tickling were unable to discriminate between objects in the NOR test not because they had a disposition towards negative affectivity, but because they had a dysfunction in specific, yet undefined, brain regions that regulate the emission of 22-kHz USVs as well as item recognition. In this regard, it is worth considering that the emission of 22-kHz USVs can be initiated by the activation of cholinergic transmission at the level of the lateral septum [32,33], and that an impaired object discrimination has been reported in rats that were evaluated in the NOR test after the infusion of pregnenolone in the lateral septum [34]. Hence, we may speculate that an altered function of the lateral septum could be a common mechanism that may explain why rats that emitted mostly 22-kHz USVs in response to tickling also displayed an impaired performance in the NOR test, although the neurochemical events underlying this possible mechanism appear ill defined.…”

Section: Discussionmentioning

confidence: 99%

Association between Novel Object Recognition/Spontaneous Alternation Behavior and Emission of Ultrasonic Vocalizations in Rats: Possible Relevance to the Study of Memory

2021

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Rats emit ultrasonic vocalizations (USVs) in situations with emotional valence, and USVs have also been proposed as a marker for memories conditioned to those situations. This study investigated whether USV emissions can predict and/or be associated with the behavior of rats in tests that evaluate unconditioned memory. To this end, rats were subjected to “tickling”, a procedure of heterospecific play that has emotional valence and elicits the emission of USVs, and afterwards evaluated in the novel object recognition test (NOR) and in the single trial continuous spontaneous alternation behavior (SAB) test in a Y-maze. The number of 22-kHz USVs (aversive) and 50-kHz USVs (appetitive) emitted in response to tickling and during NOR and SAB tests were scored, and the correlations among them and with rats’ behavior evaluated. Rats emitted 50-kHz USVs, but not 22-kHz USVs, during the NOR and SAB tests, and such calling behavior was not linked with the behavioral readouts indicative of memory function in either test. However, rats that prevalently emitted 22-kHz USVs in response to tickling displayed an impaired NOR performance. These findings suggest that measuring the emission of USVs could be of interest in studies of unconditioned memory, at least with regard to 22-kHz USVs.

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Dissimilar interaction between dopaminergic and cholinergic systems in the initiation of emission of 50-kHz and 22-kHz vocalizations

Cited by 17 publications

References 96 publications

Individual Differences in Conditioned Fear and Extinction in Female Rats

Individual Differences in Conditioned Fear and Extinction in Female Rats

Biological Functions of Rat Ultrasonic Vocalizations, Arousal Mechanisms, and Call Initiation

Association between Novel Object Recognition/Spontaneous Alternation Behavior and Emission of Ultrasonic Vocalizations in Rats: Possible Relevance to the Study of Memory

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