As late as 2003, manufacturers of ultrasonic devices were pursued by the US Federal Trade Commission and ordered at least one company to cease and desist from making unsubstantiated claims for their product. Yet, apparently provided that claims of effectiveness against rats, mice and other pests are avoided a multitude of ultrasonic products continue to be offered over the internet.
The importance of communication by vocalizations in rat infants may be further demonstrated by experiments showing that pups with less maternal help than usual were more anxious and emitted more infantile ultrasonic vocalizations than controls when they were separated from their mother and litter [43]. Additionally, experimental daily 30 min maltreatment of pups caused increased emission of their isolation calls as compared to pups receiving expected maternal care, and this procedure caused detectable epigenetic changes in the development of the brains of the maltreated rats [44]. Moreover, rats selected for higher emotionality traits emitted more ultrasonic calls when isolated as compared to pups with lower emotionality [45]. With the prolonged separation of pups from their mother, the acoustic parameters of their vocalization changed, and the pups emitted a larger proportion of high sound frequencies than the controls [46,47].
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In rats, short-duration vocalizations, classified as flat 50 kHz calls, are used as contact calls and are emitted toward familiar conspecifics, even if these conspecifics are not present nearby [60,61,62]. Rats will particularly emit these calls when they detect fresh olfactory traces of other rats, and the more scent traces they detect, the more calls they emit, usually of a frequency-modulated type [63]. In the case of possible contact with many individuals, these calls may also play another, affiliative function (see below). It was also reported that rats may emit contact vocalizations in dyadic interactions or when being alone in a cage without detectable traces of other rats but shortly after separation from other companions [60,61].
It was also suggested that during play behavior (both in juvenile and adult rats), the emission of 50 kHz calls may not only be a play signal but also an appeasement signal that de-escalates agonistic behavior during play and prevents aggressive outcomes, which can happen particularly in playing rats that are unfamiliar to each other [99,138].
This experiment, however, could not fully explain the mechanism of the vocal transmission of feeding information in rats, and the possibility of the vocal transmission of food preferences was recently raised again [164]. Some clues may come from studies performed on female mice, showing that the observer mouse emits ultrasonic vocalizations toward the demonstrator mouse that has been recently fed, but these vocalizations are dependent on the motivational state of the observer. Non-deprived animals emitted more calls toward demonstrators that were fed on palatable food, while food-deprived animals vocalized more to mice that were fed on any food regardless of its palatability [165]. These calls facilitated the proximity of the mice; however, the exact motivation for the emission of these calls and their communicative value need further studies.
Behavioral analysis of the emission of 22 kHz alarm calls and audible squeals that were emitted in dangerous confrontations with predators or large mammals led to the conclusion that ultrasonic 22 kHz calls are directed to other rats and are associated with an audience effect, while audible squeals are emitted as warning calls directly to predators and other large animals (including humans) and do not require the presence of other conspecifics [173].
The understanding that rodent vocalization is produced by arousal was first clearly stated in 1974 [222]. The notion that the emission of 22 kHz ultrasonic calls in rats specifically expresses emotional arousal is also old and was postulated over 30 years ago [223,224]. In later studies, the vocal expression of emotional states in rats was confirmed for infant calls and for adults emitting 22 kHz or 50 kHz calls by many laboratories [23,30,43,214,221,225,226,227,228,229,230].
In adult rats, ultrasonic vocalizations express two different basic emotional states: an aversive state (displeasure) or appetitive state (pleasure). Each of the functions listed in Table 1 may be assigned to one or the other state (or both) and is labeled in the table as a positive or negative state. Vocal signaling in infants is interpreted as distress and the expression of an early anxiety state [23]. Early infant vocal signaling is a reflexive and automatic process because pups do not hear calls until Postnatal Day 12 [231].
Although the initiation of a positive emotional state (dopamine) functionally antagonizes the initiation of a negative emotional state (acetylcholine) in rats, these two systems do not work in a mirror-image way. 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]. The question arises as to how cholinergic stimulation can initiate a delayed rebound with an underlying dopaminergic mechanism.
Since the predominantly noradrenergic cognitive arousal maintains the awake state and vigilance [268], it is expected that this system needs to be active to allow emotional arousal to perform its function. This was demonstrated in a pharmacological experiment. During amphetamine-induced emotional arousal with the emission of vocalizations, pharmacologic antagonism of selected subtypes of receptors of the noradrenergic system significantly decreased the emission of 50 kHz calls or selectively decreased some subtypes of 50 kHz calls, such as trill calls, the most characteristic components of emotional expression [269]. In another study with the emission of 50 kHz calls by male rats in response to a female (initially present but removed for recordings), noradrenergic agonists led to an increase in the intensity and duration of ultrasonic calls while antagonists reduced the call rate, intensity, and bandwidth of 50 kHz calls [270].
The parallel development of the brain, and particularly the limbic system, is needed to develop control of behavioral responses and enable utilizing the categorical information formed in the auditory cortex and its association with behavioral situations. When the limbic system matures, rats begin to emit a repertoire of species-typical adult ultrasonic vocalizations and they abandon the juvenile isolation calls. Since the pup isolation calls represent aversive vocalizations, the natural extension of these calls (with negative valence) after weaning are mature, constant-frequency 22 kHz calls. Maintaining constant frequency within the call requires some regulatory skills that young pups do not have. These skills of keeping the frequency flat develop gradually from Postnatal Day 7. Maturation of oligodendrocytes and the beginning of the intensive myelination process in the brain occurs from Postnatal Day 7 [304]. At the same time, the duration of calls gradually increases from Day 7.
The emission of 22 kHz alarm vocalizations is the principal alarming signal in rats, which was demonstrated by the observation of the behavior of pairs of nave or fear-experienced rats. A nave or fear-experienced receiver rat was observed in contact with another demonstrator rat that was fear-conditioned to foot shock. The receiver repeated 22 kHz alarm vocalizations of the demonstrator and showed a freezing response but only when the receiver was experienced with the foot shock (although not conditioned to it). Nave rats did not repeat the alarming calls of the demonstrator. In addition to that, rats with a damaged auditory system failed to repeat the calls of the demonstrator rat, even if they were fear-experienced [331]. Thus, the emission of 22 kHz ultrasonic calls is the main vehicle for the social transmission of anxiety; however, learning is needed for the proper recognition of the danger signaled by 22 kHz alarm calls [331].
Perception and recognition of the aversive value of 22 kHz alarming calls produced by adult rats significantly enhanced the acoustic startle response (an index of the anxiety-type emotional response) of adult receiver rats but garnered weak response from these rats if the emissions of alarming 22 kHz calls originated from young rats [332]. This result may further imply that the structure or pattern of emissions of 22 kHz calls by experienced rats contain some additional signaling features that are recognized by the recipients and can initiate anxiety in them.
The direct physiological evidence for hedonia comes from self-stimulation behavior, during which rats volitionally deliver electrical stimulation to their own brains, or from place-preference behavior. Using electrical brain stimulation, all brain regions that induced emission of 50 kHz vocalizations by electrostimulation (e.g., nucleus accumbens, ventral pallidum, lateral preoptic area, lateral hypothalamus, ventral tegmental area) are also known from previous studies to support vigorous self-stimulation behavior [350]. Place-preference behavior was reported after amphetamine injections that induced emission of 50 kHz vocalizations [344], confirming its hedonic nature. Despite suggestions that 50 kHz calls might be an (anxious) indicator of negative reinforcement learning [351], a recent pharmacological study has confirmed that emission of amphetamine-induced 50 kHz vocalizations reflect a hedonic state that is resistant to anxiogenic agents and, therefore, does not reflect anxiety [352]. Moreover, rats can also learn self-injection of amphetamine directly into the shell of the nucleus accumbens, further indicating hedonic nature of this activation [353]. 006ab0faaa