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

Abstract

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.

Keywords: 22 kHz calls; 50 kHz calls; anxiety; emotional arousal; evolution of vocalization; hedonia; infant isolation calls; mesolimbic cholinergic system; mesolimbic dopaminergic system; rat; ultrasonic vocalization.

Figure 1

The diagram presents a rough outline and relationship between the ascending cognitive arousal system and two emotional arousal systems in the rat brain. The cognitive arousal system (yellow arrows) originates from the locus coeruleus (LC), releases norepinephrine and targets most of the brain but particularly the neocortex. The mesolimbic aversive emotional arousal system (red arrows) originates from the laterodorsal tegmental nucleus (LT) and targets extensive limbic regions through hypothalamus (HYP) to lateral septum (SE) and releases acetylcholine. The mesolimbic appetitive emotional arousal system (blue arrows) originates from the ventral tegmental area (VT) and targets predominantly the nucleus accumbens (AC) and neighboring regions and releases dopamine. Both mesolimbic arousal systems are most probably also reaching the frontal cortex (FC). The diagram shows only the essential parts of these two emotional arousal systems, which represent relevant functional fragments of all cholinergic and dopaminergic neurons in the brain. It is clear at the first glance that the ascending emotional arousal systems are targeting predominantly subcortical limbic regions. Other abbreviations: CE—cerebellum, ME—mesencephalon, OB—olfactory bulb, PO—pons, TH—thalamus.

Figure 2

Comparison of developmental changes of duration of selected flat call (solid line) that were emitted by 3–30-day old Long–Evans rat infants with the developmental increase in the activity of choline acetyltransferase (ChAT) (dashed line) in the laterodorsal tegmental nucleus of Sprague Dawley rat pup brains. The pups’ flat calls that had peak sound frequency between 20 and 35 kHz and call duration ≥ 100 ms were selected from all emitted vocalizations in response to an air puff. There were almost no such vocalizations below the postnatal age 7, and then, 3 to 5 such flat calls were collected per day of development. Data for each point were usually collected from different pups because of the low number of emitted flat calls. The calls were measured by QML S-200 bat detector and the duration of calls were measured sonographically. The bioacoustic data are a fragment of an unpublished study that was partially reported as an abstract [305]. The measurement of ChAT activity was taken from the study by Ninomiya et al. (2001) [306]. Because the data have variable n-vales and were collected from different rat strains, the error bars were omitted. The graph shows parallel trajectories of developmental changes. Abbreviations: DU—duration of flat calls, ChAT—activity of choline acetyltransferase in the laterodorsal tegmental nucleus.