Hiroko Kagawa

Cognitive bias in rats evoked by ultrasonic vocalizations suggests emotional contagion

Emotional contagion occurs when an individual acquires the emotional state of another via social cues, and is an important component of empathy. Empathic responses seen in rodents are often explained by emotional contagion. Rats emit 50kHz ultrasonic vocalizations (USVs) in positive contexts, and emit 22kHz USVs in negative contexts. We tested whether rats show positive or negative emotional contagion after hearing conspecific USVs via a cognitive bias task. We hypothesized that animals in positive emotional states would perceive an ambiguous cue as being good (optimistic bias) whereas animals in negative states would perceive the same cue as being bad (pessimistic bias). Rats were trained to respond differently to two sounds with distinct pitches, each of which signaled either a positive or a negative outcome. An ambiguous cue with a frequency falling between the two stimuli tested whether rats interpreted it as positive or negative. Results showed that rats responded to ambiguous cues as positive when they heard the 50kHz USV (positive vocalizations) and negative when they heard the 22kHz USV (negative vocalizations). This suggests that conspecific USVs can evoke emotional contagion, both for positive and negative emotions, to change the affective states in receivers.

A simple explanation for the evolution of complex song syntax in Bengalese finches

The songs of Bengalese finches (Lonchura striata var. domestica) have complex syntax and provide an opportunity to investigate how complex sequential behaviour emerges via the evolutionary process. In this study, we suggest that a simple mechanism, i.e. many-to-one mapping from internal states onto syllables, may underlie the emergence of apparent complex syllable sequences that have higher order history dependencies. We analysed the songs of Bengalese finches and of their wild ancestor, the white-rumped munia (L. striata), whose songs are more stereotypical and simpler compared with those of Bengalese finches. The many-to-one mapping mechanism sufficiently accounted for the differences in the complexity of song syllable sequences of these two strains.

Domestication changes innate constraints for birdsong learning

Birdsongs are acquired by imitating the sounds produced by conspecifics. Within a species, songs diverge by cultural transmission, but the range of species-specific features is restricted by innate constraints. Bengalese finches (Lonchura striata var. domestica) are a domesticated strain of the wild White-rumped munia (Lonchura striata). The songs of the domesticated strain have more tonal sounds and more variable sequences than those of the wild strain. We compared the features of songs that were produced by normal birds, isolation-reared birds, and cross-fostered birds in both White-rumped munias and Bengalese finches to identify differences in the genetic and environmental factors of their songs. Factor analyses were conducted based on 17 song measurements. We found that isolated songs differed from normal and cross-fostered songs, especially in unstable prosodic features. In addition, there were significant differences in sound property of mean frequency between the two strains regardless of the rearing conditions. Thus, innate constraints that partially determine birdsong phenotypes may be altered through domestication.

Case studies of song and call learning by a hybrid Bengalese–Zebra Finch and Bengalese-fostered Zebra Finches: Assessing innate factors in vocal learning

ABSTRACT Vocal learning in birds is limited by both genetic and environmental factors. Innately determined, species-specific ranges of song parameters restrict song structures; the actual parameter values are determined by environmental inputs during learning. This is also true for some call notes. Here, we investigated the characteristics of songs and distance calls in a hybrid Bengalese–Zebra Finch and Bengalese-fostered Zebra Finches. The Bengalese-fostered Zebra Finches learned a limited part of the song elements, whereas the hybrid learned most of the foster fathers song. However, the hybrid could not learn the acoustic morphology of Bengalese distance calls as well as the fostered finches. The results suggest that the neural circuitry for song element repertoire and call acoustic morphology are independent and that hybridization and cross-fostering procedures are useful tools for investigating genetic and environmental factors in vocal learning.

Song complexity and auditory feedback in birds: a comparison between two strains of Bengalese finches with different degrees of song complexity.

In adult songbirds, the degree of dependency on audition for maintenance of stable song structure varies from species to species. To date, studies suggest that song deterioration after deafening may be related to the song complexity of the species. Bengalese finches sing songs that are composed of complex note-to-note transitions, and their songs are critically dependent on auditory feedback. Song deterioration occurs within five days of auditory deprivation surgery, much faster than in other species. In contrast, white-rumped munias, a wild strain of Bengalese finches, sing simple songs. To test the hypothesis that the degree of dependency on auditory feedback for the maintenance of song structure is related to song complexity, we deafened two adult white-rumped munias by cochlear removal. Songs of white-rumped munias changed in syntax within five days of surgery, a similar trend observed in Bengalese finches. We suggest that real-time auditory feedback is important in white-rumped munias, despite the simplicity of their song structure. The time course of song alteration by deafened adult birds not determined solely by song complexity.

Affective valence of neurons in the vicinity of the rat amygdala: Single unit activity in response to a conditioned behavior and vocal sound playback

Abstract We recorded single unit activity within and around the rat amygdala while rats were engaged in an operant task (which included both reward and aversive trials) and during playback of ultrasonic vocalizations (USVs) to determine if there existed neurons which responded to two different types of either positive contexts (i.e., water reward and positively associated 50 kHz vocalizations) or negative contexts (i.e., white noise and negatively associated 22 kHz vocalizations). Ultimately, we wanted to determine if these two contexts (operant condition task and vocal sounds) could be represented as either positive or negative in a single neuron. Neural activity in 90% of cells was modulated in response to one or more of those events. A small number of those cells showed neural responses to both the aversive operant trials and 22 kHz USVs, but did not show responses to reward operant trials or 50 kHz USVs, suggesting the activity of these neurons encodes for similar negative emotion in response to these two contexts. Some cells showed responses to either the reward trials or 50 kHz USVs, but no cells showed responses to both, suggesting that these cells do not show a common response to events associated with positive emotion. This might mean that 50 kHz vocal sounds and the operant rewards were segregated into two different categories within the neural representation at the level of the amygdala, even though it appeared that both events were associated with positive emotions in rats.

Limitations of a habituation task to demonstrate discrimination of natural signals in songbirds.

The habituation-dishabituation (HDH) paradigm is a common method used to examine animal cognition. Recent studies reported that spontaneous vocalizations could be used as an index of song familiarity and novelty in songbirds. However, these studies assigned only a few stimulus sets for all subjects, which might cause pseudoreplication. Therefore, we examined universality and general applicability of this method in Bengalese finches using a variety of stimulus sets. Seven unfamiliar conspecific songs were collected as a stimulus pool and a habituation song was randomly chosen for each subject. The subject was exposed to the habituation song repeatedly over 2h. During the test phase, the habituation song and a novel song randomly chosen from the stimulus pool were presented. We compared the degree of increase in call production during playback of those two songs. Although the degree was greater for the novel song compared with the habituation song in some birds, the trend was not consistent across all stimulus sets tested in these birds. Our results show that the HDH paradigm is not suitable to test song discrimination in songbirds unless precautions are taken to increase external validity by utilizing a variety of stimulus sets for each subject.

A PARSIMONIOUS REPRESENTATION WITH HIDDEN STATES FOR BIRDSONG SYNTAX: AN IMPLICATION TO HUMAN SYNTAX EVOLUTION

KENTARO KATAHIRA, KENTA SUZUKI, HIROKO KAGAWA, KAZUO OKANOYA, MASATO OKADA 1. ERATO, Okanoya Emotional Information Project, Japan Science Technology Agency, Wako, Saitama, 351-0198, Japan 2. Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa, Chiba, 277-8561, Japan 3. RIKEN Brain Science Institute, Wako, Saitama, 351-0198, Japan 4. Graduate School of Science and Engineering, Saitama University, Saitama, Saitama, 338-8570, Japan 5. Graduate School of Arts and Sciences, The University of Tokyo, Meguro, Tokyo, 153-8902, Japan

Rats became positive or negative states when listening to specific vocalizations

Emotional contagion is the process in which one became the same emotional states of the others via a behavioral signal, and many species use acoustic cues as this signal. For example, in human beings, emotional contagion occurs when they get emotional vocalizations of others, like laughter or crying. Likewise, rats emit 50 kHz or 22 kHz specific ultrasonic vocalizations (USVs) associated with positive or negative context. In order to measure whether these acoustic cues have the valence of attractiveness or aversiveness, we utilized the cognitive bias task in rats. Rats were trained to respond differently for two neutral stimuli. One resulted in a positive outcome while the other produced negative outcome. Then the intermediate stimulus between the two was used to test whether that was interpreted as being positive or negative. After the 50 kHz USVs stimulation, rat interpreted the neutral stimuli as being positive, while after the 22 kHz USV stimulation, the same stimuli were regarded as negative. Results...

INNATE TEMPLATE DIFFERENCE COULD INDUCE SIGNAL COMPLEXITY: A COMPARISON OF SONG FEATURES UNDER AUDITORY ISOLATION BETWEEN WILD AND DOMESTICATED FINCHES

Bird songs are acquired by vocal learning. Mechanism and evolution of birdsongs partly parallels those of human language. Songs of Bengalese finches, which are composed of complex sequence, have been studied as a key to understand evolution of signal complexity. Bengalese finches are domesticated from wild white-rumped munias. Songs of domesticated finches contain more tonal sounds and complex note-to note transition than those of wild strains (Okanoya, 2004). Takahasi & Okanoya (2010) found differences in learning property between the two strains using a cross-fostering paradigm. Wild finches imitated a conspecific tutor’s song more precisely than domesticated finches do. However, domesticated finches imitated both tutor’s songs roughly equally. The domesticated strain may produce their own songs based largely on innate template. Auditory isolation experiments enable us to examine the genetic contribution to song learning. We examined the songs of isolated and normal birds from both strains in order to compare characteristics of innate templates. Isolated-birds were raised by only females from day 10 post-hutch to isolate from conspecifec songs. Then, they were housed alone in sound proof chamber from day 35. Normal birds were raised by their parents. We used six normal birds in each strain, seven isorated-birds in white rumped munias and six isorated-birds in Bengalse finches. We recorded songs at day 120, when normal leaning period is over. We analyzed 30 songs per individuals. As a result of song comparison, we found song parameter differed between isolated wild and domesticated strains (Fig.1). Pitch structure in each song note of isolated white rumped munias had higher variance than those of isolated Bengalse finches (Fig. 1). In addition, variance of pitch differed between isolated