Maki Ikebuchi

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.

Sex differences in song perception in Bengalese finches measured by the cardiac response

Abstract Birdsong may be perceived and processed differently by males and females because the production and function of this behaviour are often sexually dimorphic. However, examination of this hypothesis has been difficult, since different behavioural measures have been used to describe the perceptual process for each sex. We analysed changes in heart rate as an index of song perception in Bengalese finches, Lonchura striata var. domestica . In this species, only males sing, and song is used exclusively for mate attraction. This species is not territorial and songs are never used in aggressive contexts. In both sexes, repeated presentation of a song resulted in a waning of the heart rate response. Presentation of heterospecific songs did not increase the heart rate. When a novel conspecific song was presented, the heart rate increased only in females with each presentation of the stimulus, not in males. These results correspond to the sex differences in song usage in this species. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.

Left-side dominance for song discrimination in Bengalese finches (Lonchura striata var. domestica)

Abstract. Male Bengalese finches are left-side dominant for the motor control of song in the sensorimotor nucleus (the high vocal center, or HVc) of the telencephalon. We examined whether perceptual discrimination of songs might also be lateralized in this species. Twelve male Bengalese finches were trained by operant conditioning to discriminate between a Bengalese finch song and a zebra finch song. Before training, the left HVc was lesioned in four birds and the right HVc was lesioned in four other birds. The remaining four birds were used as controls without surgery. Birds with a left HVc lesion required significantly more time to learn to discriminate between the two songs than did birds with a right HVc lesion or intact control birds. These results suggest that the left HVc is not only dominant for the motor control of song, but also for the perceptual discrimination of song.

Developmental learning of complex syntactical song in the Bengalese finch

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.

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.

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.

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.

Limited auditory memory for conspecific songs in a non-territorial songbird.

Males of territorial songbird species have to remember a large number of conspecific songs to defend their territories, while non-territorial songbirds do not need to. A study of a territorial species suggested seemingly unlimited auditory memory size. We measured auditory memory in Bengalese finches, a non-territorial songbird species, to examine whether the auditory memory size for conspecific songs depends on the ecological requirements for song use. Five birds were trained by operant techniques to classify song stimuli into two arbitrary categories. The learning curve reached an asymptote within ∼100 sessions in all five birds and only eight songs were concurrently remembered on average. Results suggest that ecological requirements for song use are correlated with the auditory song memory capacity.

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.

Growth of pair bonding in Zebra Finches: physical and social factors

ABSTRACT We investigated the process of pair formation in Zebra Finches. Two males and two females, unfamiliar with each other, were put in a flight cage and we observed these four birds for 30 min each day for 10 days. In total, five sets of four birds were used. During the observation period, the position of each individual was recorded every minute. The occurrences of songs, agonistic behavior, and other behaviors were recorded in real time and additional video analyses were performed off line. On introducing the birds, the males immediately began fighting and a firm dominance hierarchy was established, usually within a few minutes. Most of the directed songs occurred during the first day and gradually the proportion of undirected songs increased. In each set, birds formed at least one intimate heterosexual pair. We analyzed the properties of the individuals that formed the pair. The results indicated that the heavier females pair-bonded quicker, and the males that won dominance bonded sooner and four out of five dominant males weighed more than the other male in each set. By contrast, the song duration and song quality of each male did not differ between the paired male and the other male. In our experimental setting, females did not pay as much attention to the song as to the social dominance. Therefore, the functional significance of courtship songs appears after the dominance hierarchy is established among males and is used as a secondary cue for mate choice in females.