Ethotransmission: communication of emotional states through ultrasonic vocalization in rats
TL;DR: Species-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.
About: This article is published in Current Opinion in Neurobiology.The article was published on 2013-06-01. It has received 356 citations till now.
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TL;DR: This review focuses on current standards, i.e. state-of-the-art behavioural phenotyping tasks to assess autism core symptoms in rodent models, plus a number of new developments in the behavioural domains of social facilitation, observational learning, and empathy, including an autism severity score, scent marking behaviour as an additional, ethologically valid measure for communication.
180 citations
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...First of all, rats are highly social animals, showing various types of social behaviours and using a rich acoustic communication system (for reviews see: [75,85])....
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TL;DR: In a new model, male rats approach stressed juveniles but avoid stressed adults; these behaviors require excitatory action of oxytocin within the insular cortex, which implicateinsular cortex as a key component in the circuit underlying age-dependent social responses to stressed conspecifics.
Abstract: Social animals detect the affective states of conspecifics and utilize this information to orchestrate social interactions. In a social affective preference text in which experimental adult male rats could interact with either naive or stressed conspecifics, the experimental rats either approached or avoided the stressed conspecific, depending upon the age of the conspecific. Specifically, experimental rats approached stressed juveniles but avoided stressed adults. Inhibition of insular cortex, which is implicated in social cognition, and blockade of insular oxytocin receptors disrupted the social affective behaviors. Oxytocin application increased intrinsic excitability and synaptic efficacy in acute insular cortex slices, and insular oxytocin administration recapitulated the behaviors observed toward stressed conspecifics. Network analysis of c-Fos immunoreactivity in 29 regions identified functional connectivity between insular cortex, prefrontal cortex, amygdala and the social decision-making network. These results implicate insular cortex as a key component in the circuit underlying age-dependent social responses to stressed conspecifics.
161 citations
TL;DR: A framework for play signals is provided, showing that they range along two dimensions: one from signals borrowed from other functional contexts to those that are unique to play, and the other from purely emotional expressions to highly cognitive (intentional) constructions.
Abstract: Rough-and-tumble play (RT) is a widespread phenomenon in mammals. Since it involves competition, whereby one animal attempts to gain advantage over another, RT runs the risk of escalation to serious fighting. Competition is typically curtailed by some degree of cooperation and different signals help negotiate potential mishaps during RT. This review provides a framework for such signals, showing that they range along two dimensions: one from signals borrowed from other functional contexts to those that are unique to play, and the other from purely emotional expressions to highly cognitive (intentional) constructions. Some animal taxa have exaggerated the emotional and cognitive interplay aspects of play signals, yielding admixtures of communication that have led to complex forms of RT. This complexity has been further exaggerated in some lineages by the development of specific novel gestures that can be used to negotiate playful mood and entice reluctant partners. Play-derived gestures may provide new mechanisms by which more sophisticated communication forms can evolve. Therefore, RT and playful communication provide a window into the study of social cognition, emotional regulation and the evolution of communication systems.
146 citations
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...It has yet to be determined whether these calls are performed specifically to solicit play or are simply a reflection of positive mood, although there is growing evidence suggesting that ultrasonic vocalizations (USVs) may also have communicative properties during emotionally charged behaviours (Brudzynski, 2013)....
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...…determined whether these calls are performed specifically to solicit play or are simply a reflection of positive mood, although there is growing evidence suggesting that ultrasonic vocalizations (USVs) may also have communicative properties during emotionally charged behaviours (Brudzynski, 2013)....
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TL;DR: The diversity of numerous aetiological factors and the alterations in variety of neurotransmitter generation, release and function linked to ASD are discussed with focus on drugs currently used to manage neuropsychiatric symptoms related to ASD.
Abstract: Autistic Spectrum Disorder (ASD) is a complex neurodevelopmental brain disorder characterized by two core behavioral symptoms, namely impairments in social communication and restricted/repetitive behavior. The molecular mechanisms underlying ASD are not well understood. Recent genetic as well as non-genetic animal models contributed significantly in understanding the pathophysiology of ASD, as they establish autism-like behavior in mice and rats. Among the genetic causes, several chromosomal mutations including duplications or deletions could be possible causative factors of ASD. In addition, the biochemical basis suggests that several brain neurotransmitters, e.g., dopamine (DA), serotonin (5-HT), gamma-amino butyric acid (GABA), acetylcholine (ACh), glutamate (Glu) and histamine (HA) participate in the onset and progression of ASD. Despite of convincible understanding, risperidone and aripiprazole are the only two drugs available clinically for improving behavioral symptoms of ASD following approval by Food and Drug Administration (FDA). Till date, up to our knowledge there is no other drug approved for clinical usage specifically for ASD symptoms. However, many novel drug candidates and classes of compounds are underway for ASD at different phases of preclinical and clinical drug development. In this review, the diversity of numerous aetiological factors and the alterations in variety of neurotransmitter generation, release and function linked to ASD are discussed with focus on drugs currently used to manage neuropsychiatric symptoms related to ASD. The review also highlights the clinical development of drugs with emphasis on their pharmacological targets aiming at improving core symptoms in ASD.
127 citations
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...Notably, rat has become the most extensively used animals in the context of SCH and ASD neuroscience (Brudzynski, 2013)....
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...Accordingly, and as compared to mice, rats provide more experimental advantages including the fact that rats demonstrate richer social behavioral skills, show various types of social behaviors, and use a rich CNS communication system (Brudzynski, 2013)....
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TL;DR: The results support the hypothesis that these call types are processed in distinct neuroanatomical regions and establish a functional link between pro-social communicative signals and reward-related neurotransmission.
Abstract: Rats emit ultrasonic vocalizations (USVs) that are thought to serve as situation-dependent affective signals and accomplish important communicative functions. In appetitive situations, rats produce 50 kHz USVs, whereas 22 kHz USVs occur in aversive situations. Reception of 50 kHz USVs induces social approach behavior, while 22 kHz USVs lead to freezing behavior. These opposite behavioral responses are paralleled by distinct brain activation patterns, with 50 kHz USVs, but not 22 kHz USVs, activating neurons in the nucleus accumbens (NAcc). The NAcc mediates appetitive behavior and is critically modulated by dopaminergic afferents that are known to encode the value of reward. Therefore, we hypothesized that 50 kHz USVs, but not 22 kHz USVs, elicit NAcc dopamine release. While recording dopamine signaling with fast-scan cyclic voltammetry, freely moving rats were exposed to playback of four acoustic stimuli via an ultrasonic speaker in random order: (1) 50 kHz USVs, (2) 22 kHz USVs, (3) time- and amplitude-matched white noise, and (4) background noise. Only presentation of 50 kHz USVs induced phasic dopamine release and elicited approach behavior toward the speaker. Both of these effects, neurochemical and behavioral, were most pronounced during initial playback, but then declined rapidly with subsequent presentations, indicating a close temporal relationship between the two measures. Moreover, the magnitudes of these effects during initial playback were significantly correlated. Collectively, our findings show that NAcc dopamine release encodes pro-social 50 kHz USVs, but not alarming 22 kHz USVs. Thus, our results support the hypothesis that these call types are processed in distinct neuroanatomical regions and establish a functional link between pro-social communicative signals and reward-related neurotransmission.
126 citations
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...These calls are thought to serve as situation-dependent affective signals and accomplish important communicative functions (Portfors, 2007; Brudzynski, 2013; Wöhr and Schwarting, 2013)....
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References
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TL;DR: Experiments suggest that dopaminergic neurons localized in the posteromedial ventral tegmental area (VTA) and central linear nucleus raphe selectively project to the ventromedial striatum (medial olfactory tubercle and medial nucleus accumbens shell), whereas the anteromedial VTA has few if any projections to the vents of the ventral striatum.
1,387 citations
"Ethotransmission: communication of ..." refers background in this paper
...The ascending dopamine fibers originate from the ventral tegmental area [47,48] (Figure 2, VTA)....
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TL;DR: Converging ethological, pharmacological, and brain stimulation research indicates that whereas long low-frequency USVs occur during anticipation of punishment or avoidance behavior, short, high-frequency (< 0.3-s, approximately 50-kHz) USVs typically occur during expectation of reward or approach behavior, which suggests that long 22-kHz USVs may index a state of negative activation, whereas short, 50- kHzUSVs may instead index astate of positive activation.
Abstract: Adult rats spontaneously vocalize in ultrasonic frequencies. Although these ultrasonic vocalizations (USVs) have been described as by-products of locomotor activity or social signals, accumulating evidence suggests that they may also index anticipatory affective states. Converging ethological, pharmacological, and brain stimulation research indicates that whereas long low-frequency (> 0.3-s, approximately 22-kHz) USVs occur during anticipation of punishment or avoidance behavior, short, high-frequency (< 0.3-s, approximately 50-kHz) USVs typically occur during anticipation of reward or approach behavior. Thus, long 22-kHz USVs may index a state of negative activation, whereas short, 50-kHz USVs may instead index a state of positive activation. This hypothesis has theoretical implications for understanding the brain circuitry underlying mammalian affective states and clinical applicability for modeling hedonic properties of different psychotropic compounds.
579 citations
"Ethotransmission: communication of ..." refers background in this paper
...The 22 kHz vocalizations are emitted in negative states and aversive situations, while 50 kHz calls are emitted in positive states and appetitive situations [21–23]....
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TL;DR: The results suggest that the production of ultrasonic vocalizations during and after exposure to a predator is greatly facilitated by the presence of familiar conspecifics, and may serve as alarm cries.
424 citations
TL;DR: Low frequency recordings of ultrasonic vocalizations made during mating, aggression, and both conspecific and heterospecific rough-and-tumble play behavior suggest that frequency modulated 50-kHz calls index a positively valenced, appetitive, social-emotional state in rats.
Abstract: Rats (Rattus norvegicus) emit a variety of ultrasonic vocalizations throughout their lifespan that reflect different forms of emotional arousal and accompanying affective states. In this study, high frequency recordings of ultrasonic vocalizations were made during mating, aggression, and both conspecific and heterospecific (dubbed “tickling”) rough-and-tumble play behavior. We found that frequency modulated 50-kHz calls (trills and step calls) were positively correlated with positively valenced appetitive behavior during mating, play, and aggression. These calls were also positively correlated with the reward value of these social encounters. However, constant frequency (i.e., flat) 50-kHz calls were not related to appetitive behaviors or reward. In contrast, 22-kHz calls were positively related to aversive/withdrawal behaviors during mating, play, and aggression. Finally, we found that rats self-administered playback of frequency modulated 50-kHz trill calls and avoided playback of 22-kHz calls. Playback of flat 50-kHz calls or tape hiss was neutral. These results suggest that frequency modulated 50-kHz calls index a positively valenced, appetitive, social-emotional state in rats.
399 citations
TL;DR: Some of the historical arguments that led to the social complexity hypothesis are described, and evidence in support of the hypothesis is reviewed, to discuss social complexity as a driver of communication and possible causal factor in human language origins.
Abstract: The 'social complexity hypothesis' for communication posits that groups with complex social systems require more complex communicative systems to regulate interactions and relations among group members. Complex social systems, compared with simple social systems, are those in which individuals frequently interact in many different contexts with many different individuals, and often repeatedly interact with many of the same individuals in networks over time. Complex communicative systems, compared with simple communicative systems, are those that contain a large number of structurally and functionally distinct elements or possess a high amount of bits of information. Here, we describe some of the historical arguments that led to the social complexity hypothesis, and review evidence in support of the hypothesis. We discuss social complexity as a driver of communication and possible causal factor in human language origins. Finally, we discuss some of the key current limitations to the social complexity hypothesis-the lack of tests against alternative hypotheses for communicative complexity and evidence corroborating the hypothesis from modalities other than the vocal signalling channel.
397 citations
"Ethotransmission: communication of ..." refers background in this paper
...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]....
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