Ethotransmission: communication of emotional states through ultrasonic vocalization in rats

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Adult rats emit two categories of ultrasonic vocalizations, 22 kHz calls and 50 kHz calls. These vocalizations communicate animal's emotional state to other members of the social group. Production of social vocalizations is an evolutionary old activity in vertebrates, and is regulated by well-preserved brain circuitries. The 22 kHz calls express negative, aversive state and are initiated by activity of the mesolimbic cholinergic system originating from laterodorsal tegmental nucleus. The 50 kHz calls express positive, appetitive state and are initiated by activity of the mesolimbic dopaminergic system originating from the ventral tegmental area. The 22 kHz calls serve as warning and alarm calls, while the 50 kHz calls serve as affiliative and social-cooperating calls. These specie-specific vocalizations play role of ethological transmitters, termed ethotransmitters, that is, they are species-specific signals that are selectively recognized by receivers and have capability of changing emotional state of the receivers.

Highlights

► The ascending mesolimbic cholinergic system initiates negative emotional state. ► The ascending mesolimbic dopaminergic system initiates positive emotional state. ► The negative and positive states are signaled by 22 kHz and 50 kHz vocalizations. ► State-specific vocalizations can change emotional state of the recipients. ► Species-specific signals changing state of recipients are ethotransmitters.

Introduction

Research of the last 25 years has proven that rats are a highly vocal species and their vocalizations are an inseparable concomitants of their well-developed social life (for review see [1, 2, 3]). Almost all frequently observed, social vocalizations are emitted in the ultrasonic range of sound frequencies (i.e. above 20 kHz) in a variety of behavioral situations of both aversive or appetitive nature. Rats use the larynx for production of ultrasonic vocalizations and have developed a vocal mechanism allowing them to use the larynx with constricted focal folds as an ultrasonic whistle [4, 5•]. These vocalizations serve rats for short-range within-colony communication and they seem to be particularly suitable for communication in the underground burrows [6]. On the ground surface, it is difficult to localize the animal emitting ultrasounds, particularly in the environment covered with vegetation [6], so these calls serve usually an alarming purpose in the open spaces. These observations support the view that ultrasonic vocalization is of considerable biological significance for rats and serves as communication tool [7]. Emission of ultrasonic calls increases cohesiveness of the social group, and as recent studies suggest, the ultrasonic communication can transmit emotional state to conspecifics and it enables development and enhancement of cooperative behavior among rats [7, 8••].

Emission of ultrasonic vocalizations by the rat larynx does not represent a passive whistling process but a well-regulated production of structured ultrasonic sounds that depends on a centrally controlled activity of cricothyroid and thyroarytenoid laryngeal muscles [5]. Activity of laryngeal muscles is regulated by central pattern generators for vocalization that are located in the caudal hindbrain and rostral spinal cord in all vocal vertebrates [9, 10•]. Thus, production of social vocalizations is an evolutionary old activity, and it is regulated by well-preserved brain circuitries. This communication is an adaptation of a high biological significance that developed over a long phylogenetic history of vertebrates.

Adaptive benefits of vocal communication are relevant to a long list of basic motivated behaviors including sexual behavior, agonistic behavior (offensive or defensive behavior), avoidance behavior (avoiding dangers), seeking rewards, playing (ludic behavior), etc. A common denominator of all of these behaviors is their emotional nature, that is, increased arousal, prolonged attention, heightened motor activity, increased activity of the autonomic and endocrine systems, certain intensity and persistence of responses, and periodicity of these behaviors [11]. Thus, the common role of vocalizations emitted during most of these behaviors may be described as expression or communication of animal emotional state to other members of the social group [12]. A trait of communicating emotional states to conspecifics has been clearly enhanced by natural selection. Vocal expression of emotional states is equally important in simple mother-infant communication [13, 14] as in vocal communication within larger mammalian social groups in adulthood [15]. Vocal communication becomes richer and more intricate with growing size of the social group and group internal complexity, as it was shown for many mammalian species [16, 17] and for birds [18].

Section snippets

What emotional states are communicated by rats to conspecifics?

Although, there is a multitude of states of the organism (for a full definition of the state of the organism, see [12]), they can be classified and organized according to external biological situations, in which they occur (e.g. danger), or internal organismal conditions (e.g. illness). Basic emotional states, however, can be divided into two fundamental classes arbitrarily termed positive and negative states, which are common to all animals. ‘The negative state is evoked by external or

Conclusions

Two tegmental ascending systems, mesolimbic dopaminergic and mesolimbic cholinergic system, are responsible for the initiation of positive or negative emotional states with concurrent emission of state-specific ultrasonic vocalization in rats. Release of acetylcholine in the medial cholinoceptive vocalization strip — the target area for the ascending cholinergic system — generates the negative state with emission of 22 kHz vocalizations. Release of dopamine in the shell of the nucleus accumbens

Definition of some terms

Cholinoceptive — A pharmacological feature pertaining to receptors, neurons, brain structures, or organs of being receptive and responsive to action of acetylcholine or acetylcholine agonists.

Bandwidth — The difference between the highest and the lowest sound frequency within the vocalization signal; the frequency band of a single call.

Ethotransmitter — Species-specific animal-originating signal (here vocalization) produced by a specialized organ (larynx), decoded selectively by the brain of

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

The research topic of this review and preparation of the manuscript were funded by a Discovery Grant to the author, as Principal Investigator, from the Natural Sciences and Engineering Research Council of Canada. The author would like to thank Mr. Michael Silkstone, MSc, for his help in preparation of Figure 1.

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