Different Reactions of Zebra Finches and Bengalese Finches to a Three-Component Mixture of Anesthetics.

Kawai et al. (2011) recently introduced a mixture of three anesthetic agents (here called MMB) that has an effect similar to ketamine/xylazine in mice, which might allow more effective reaction to changes in the animal condition, as an antagonist is available, and which can be used without license for handling narcotic drugs. Using Kawai's study as a baseline, we tested whether this anesthesia and its antagonist can also be used in avian studies. In the present study, we used two species, the zebra finch and the Bengalese finch, of the avian family Estrildidae. In zebra finches, anesthesia effects similar to the use of ketamine/xylazine and to those obtained in mice can be reached by the use of MMB if a higher dose is applied. MMB leads to more variable anesthesia, but has the advantage of a longer time window of deep anesthesia. An antagonist to one component of MMB reduced the awaking time, but was not as effective as in mice. For Bengalese finches, MMB cannot be generally recommended because of difficult handling and high mortality rate when used without antagonist, but could be used for perfusions instead of pentobarbital.

Chick Development and Asynchroneous Hatching in the Zebra Finch (Taeniopygia guttata castanotis).

The mode of hatching in birds has important impacts on both parents and chicks, including the costs and risks of breeding for parents, and sibling competition in a clutch. Birds with multiple eggs in a single clutch often begin incubating when most eggs are laid, thereby reducing time of incubation, nursing burden, and sibling competition. In some songbirds and some other species, however, incubation starts immediately after the first egg is laid, and the chicks thus hatch asynchronously. This may result in differences in parental care and in sibling competition based on body size differences among older and younger chicks, which in turn might produce asynchronous development among siblings favoring the first hatchling, and further affect the development and fitness of the chicks after fledging. To determine whether such processes in fact occur in the zebra finch, we observed chick development in 18 clutches of zebra finches. We found that there were effects of asynchronous hatching, but these were smaller than expected and mostly not significant. Our observations suggest that the amount of care given to each chick may be equated with such factors as a camouflage effect of the down feathers, and that the low illumination within the nest also complicates the determination of the hatching order by the parents.

Auditory Responses to Vocal Sounds in the Songbird Nucleus Taeniae of the Amygdala and the Adjacent Arcopallium.

Many species of animals communicate with others through vocalizations. Over time, these species have evolved mechanisms to respond to biologically relevant vocal sounds via adaptive behaviors. Songbirds provide a good opportunity to search for the neural basis of this adaptation, because they interact with others through a variety of vocalizations in complex social relationships. The nucleus taeniae of the amygdala (TnA) is a structure located in the ventromedial arcopallium, which is akin to the mammalian medial amygdala. Studies on the anatomy and function of this nucleus have led to the speculation that the TnA is one of the possible neural substrates that represents the relevance of acoustic stimuli related to behavior. However, neural responses in this nucleus to auditory stimuli have not been studied in depth. To give a detailed description about auditory responses of the TnA in the songbird, we conducted neural recordings from the TnA and the adjacent arcopallium in adult male and female Bengalese finches under anesthesia. The birds were exposed to auditory stimuli including natural vocalizations as well as synthesized noise. We demonstrated that a substantial population of neurons in the TnA and the adjacent arcopallium responded to vocal sounds and that some neurons were selectively activated to specific stimuli. Proportions of responsive cells and stimulus-selective cells were larger in males than in females. In addition, a larger ratio of selective cells was observed in the arcopallium compared to the TnA. These findings support the idea that neuronal activity in the TnA and the neighboring area represents behavioral relevance of sounds. Further studies in electrophysiology combined with evidence from other fields, such as region-specific gene expression patterns, are required to fully understand the functions of the TnA as well as the evolution of the amygdala in songbirds and vertebrate animals.

Very early development of nucleus taeniae of the amygdala.

The avian nucleus taeniae of the amygdala (TnA) corresponds to part of the mammalian medial amygdala. Like its mammalian counterpart, it has been shown to be involved in the control of social function. According to behavioral observations, such control is already necessary early in the ontogenetic development of a bird. If so, TnA should be one of the earliest differentiating brain structures of the telencephalon. Our anatomical study shows that TnA can already be delineated at posthatching day one. The volume of TnA exhibits a growth spurt between days 1 and 8 posthatch, developing at a faster rate than the entire telencephalon. Our results suggest that between days 1 and 8 the growth of neuropil exceeds the enhancement of neuron number (leading to a decrease of cell density), and an addition at the same pace of new neurons and neuropil thereafter. A plateau is reached at posthatch day 30. The development of TnA precedes that of the song control nuclei and is similar to the early growth of thalamic and telencephalic sensory areas. This adds to the idea that this structure may already be involved in social control at the time of hatching. A proximate cause of the early development of TnA might be the direct afference from the olfactory bulb.

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.

Sex differences in the development and expression of a preference for familiar vocal signals in songbirds.

Production and perception of birdsong critically depends on early developmental experience. In species where singing is a sexually dimorphic trait, early life song experience may affect later behavior differently between sexes. It is known that both male and female songbirds acquire a life-long memory of early song experience, though its function remains unclear. In this study, we hypothesized that male and female birds express a preference for their fathers' song, but do so differently depending on the developmental stage. We measured preference for their father's song over an unfamiliar one in both male and female Bengalese finches at multiple time points across ontogeny, using phonotaxis and vocal response as indices of preference. We found that in males, selective approach to their father's song decreased as they developed while in females, it remained stable regardless of age. This may correspond to a higher sensitivity to tutor song in young males while they are learning and a retained sensitivity in females because song is a courtship signal that is used throughout life. In addition, throughout development, males vocalized less frequently during presentation of their father's song compared to unfamiliar song, whereas females emitted more calls to their father's song. These findings contribute to a deeper understanding of why songbirds acquire and maintain such a robust song memory.

Effects of domestication on neophobia: A comparison between the domesticated Bengalese finch (Lonchura striata var. domestica) and its wild ancestor, the white-rumped munia (Lonchura striata).

Bengalese finches (Lonchura striata var. domestica) have more complex song traits than their wild ancestors, white-rumped munias (Lonchura striata). Domesticated finches are likely able to allocate more resources to reproduction (e.g. singing) rather than to mechanisms intended for coping with predation, which are no longer needed under domesticated conditions. Here, we aimed to examine the effects of changes in selection pressure due to domestication on the behaviour of Bengalese finches and to contemplate the possible evolutionary mechanisms underlying these changes. To do so, we compared neophobic responses to novel-object conditions as an assessment of reactions to potential predators. We studied groups of Bengalese finches and white-rumped munias and found that Bengalese finches were more likely to eat the food provided to them under novel-object conditions. Bengalese finches had a shorter latency time to eat, and this latency time was less affected by the novel object in the case of Bengalese finches compared to white-rumped munias. Therefore, Bengalese finches have reduced neophobic responses due to domestication. The behavioural strategies of white-rumped munias appear to be more suitable for natural environments, which include unpredictable risks, whereas Bengalese finches have likely adapted their behaviour to the conditions of artificial selection.

Neural correlates of vocal initiation in the VTA/SNc of juvenile male zebra finches.

Initiation and execution of complex learned vocalizations such as human speech and birdsong depend on multiple brain circuits. In songbirds, neurons in the motor cortices and basal ganglia circuitry exhibit preparatory activity before initiation of song, and that activity is thought to play an important role in successful song performance. However, it remains unknown where a start signal for song is represented in the brain and how such a signal would lead to appropriate vocal initiation. To test whether neurons in the midbrain ventral tegmental area (VTA) and substantia nigra pars compacta (SNc) show activity related to song initiation, we carried out extracellular recordings of VTA/SNc single units in singing juvenile male zebra finches. We found that a subset of VTA/SNc units exhibit phasic activity precisely time-locked to the onset of the song bout, and that the activity occurred specifically at the beginning of song. These findings suggest that phasic activity in the VTA/SNc represents a start signal that triggers song vocalization.

Arousal State-Dependent Alterations in Neural Activity in the Zebra Finch VTA/SNc.

Sleep-wake behaviors are important for survival and highly conserved among animal species. A growing body of evidence indicates that the midbrain dopaminergic system is associated with sleep-wake regulation in mammals. Songbirds exhibit mammalian-like sleep structures, and neurons in the midbrain ventral tegmental area (VTA) and substantia nigra pars compacta (SNc) possess physiological properties similar to those in mammals. However, it remains uncertain whether the neurons in the songbird VTA/SNc are associated with sleep-wake regulation. Here, we show that VTA/SNc neurons in zebra finches exhibit arousal state-dependent alterations in spontaneous neural activity. By recording extracellular single-unit activity from anesthetized or freely behaving zebra finches, we found that VTA/SNc neurons exhibited increased firing rates during wakefulness, and the same population of neurons displayed reduced firing rates during anesthesia and slow-wave sleep. These results suggest that the songbird VTA/SNc is associated with the regulation of sleep and wakefulness along with other arousal regulatory systems. These findings raise the possibility that fundamental neural mechanisms of sleep-wake behaviors are evolutionarily conserved between birds and mammals.

Amygdala and socio-sexual behavior in male zebra finches.

Neuroanatomical studies including pathway tracing and cytochemical characterizations have suggested that the avian nucleus taeniae of the amygdala (TnA) might be homologous to a part of the mammalian medial amygdala. Recent behavioral observations in TnA-lesioned birds also reported deficits in the control of motivational aspects of behavior, advancing the concept of homology of the structure in the two classes of animals. To further examine the functional role of TnA, we used a highly social, monogamous song bird species, the zebra finch, for our experiments. Male birds received a focal lesion of TnA, and several aspects of socio-sexual behavior of these animals were compared with control bird behavior. We found that zebra finch males with TnA lesions were never chosen as sexual partners by a female in a triadic situation with another male because they showed less sexually motivated behavior. Because such sexually motivated behavior was shown in dyadic situations with a lesioned male and a female, however, and females in this situation also showed pair bonding behavior towards the lesioned males, TnA might be involved in other behaviors, not just sexual behavior towards females. Instead, it might play a role in the control of a variety of social encounters including male-female and male-male interactions. This research clearly indicates that TnA, by its involvement in the control of socio-sexual behavior, is functionally comparable with the mammalian medial amygdala.

Dynamic changes in level influence spatial coding in the lateral superior olive.

It is well established that the responses of binaural auditory neurons can adapt and change dramatically depending on the nature of a preceding sound. Examples of how the effects of ensuing stimuli play a functional role in auditory processing include motion sensitivity and precedence-like effects. To date, these types of effects have been documented at the level of the midbrain and above. Little is known about sensitivity to ensuing stimuli below in the superior olivary nuclei where binaural response properties are first established. Here we report on single cell responses in the gerbil lateral superior olive, the initial site where sensitivity to interaural level differences is established. In contrast to our expectations we found a robust sensitivity to ensuing stimuli. The majority of the cells we tested (86%), showed substantial suppression and/or enhancement to a designated target stimulus, depending on the nature of a preceding stimulus. Hence, sensitivity to ensuing stimuli is already established at the first synaptic station of binaural processing.

Developmental learning of complex syntactical song in the Bengalese finch: a neural network model.

We developed a neural network model for studying neural mechanisms underlying complex syntactical songs of the Bengalese finch, which result from interactions between sensori-motor nuclei, the nucleus HVC (HVC) and the nucleus interfacialis (NIf). Results of simulations are tested by comparison with the song development of real young birds learning the same songs from their fathers. The model shows that complex syntactical songs can be reproduced from the simple interaction between the deterministic dynamics of a recurrent neural network and random noise. Features of the learning process in the simulations show similar trends to those observed in empirical data on the song development of real birds. These observations suggest that the temporal note sequences of songs take the form of a dynamical process involving recurrent connections in the network of the HVC, as opposed to feedforward activities, the mechanism proposed in the previous model.

Spatiotemporal properties of visual stimuli for song induction in Bengalese finches.

Male Bengalese finches sing directed songs in response to video images of females projected onto a thin-film transistor monitor. We used this experimental paradigm to elucidate which properties of visual stimuli are important for eliciting singing. When video recordings of female Bengalese or zebra finches were used as visual stimuli, only images of conspecific females elicited singing from male Bengalese finches. When images of female Bengalese finches were rotated by 0 degrees, 90 degrees, or 180 degrees, only the upright images elicited singing. Finally, temporally normal (forward playback) images were more effective than time-reversed images and still images for eliciting singing. These results suggest that both the spatial and temporal arrangements of visual stimuli affect the singing behavior of male finches.

Behavioral and neural trade-offs between song complexity and stress reaction in a wild and a domesticated finch strain.

The Bengalese finch is the domesticated strain of the wild white-rumped munia. Bengalese finches have been domesticated and reproductively isolated for over 250 years from the wild strain. During this period, the courtship songs of the domesticated birds became phonologically and syntactically complex. In addition, psychological and physiological stress reactions to environmental and social factors diverged between the two strains. Based on our behavioral and histological studies, we consider the balance between the glucocorticoid- and mineralocorticoid receptors in song control nuclei and in the avian amygdala as to determine whether a bird can develop complex songs or rather has to devote the neural resources for the maintenance of stress reactions. We therefore suggest that phonological and syntactical complexity in Bengalese finch songs initially evolved because domestication freed them from species recognition and environmental stress, and then sexual selection increased the complexity. Neural and molecular studies also support the notion that Bengalese finches keep more song plasticity as adults. In conclusion, the present study suggests that domestication changed factors related with psychobiology of stress reactions and learning in finches.

The impact of domestication on fearfulness: a comparison of tonic immobility reactions in wild and domesticated finches.

We examined differences in the fear response between Bengalese finches and their wild ancestor, the white-backed munia, to explore the evolutionary mechanisms of behavioural changes due to domestication. The Bengalese finch (Lonchura striata var. domestica) was domesticated from the wild-living white-backed munia (L. striata) approximately 250 years ago. A previous study indicated that Bengalese finches sing much more complex songs than white-backed munias. We hypothesised that Bengalese finches are likely able to allocate more resources to reproduction in exchange for reduced survival effort. We measured tonic immobility (TI) reactions as a response to physical restraint to evaluate fearfulness related to coping with predation. The results showed that Bengalese finches exhibited decreased TI responses compared with white-backed munias. TI responses were unaffected by sex, body weight or growth conditions. These differences suggest that the fearfulness in Bengalese finches has been reduced by selective pressure during domestication. Bengalese finches may have been able to increase the investment of energy in reproduction in exchange for reduced costs of predation and coping necessary to survive in the wild; these behavioural changes may have been a major target of domestication effects in this species.