Isolation-dependent enhancement of 2-[14C]deoxyglucose uptake in the forebrain of zebra finch males

In a previous study (H. J. Bischof & K. Herrmann (1986), Behavioral Brain Research, 21, 215-221) we demonstrated that four forebrain areas of the zebra finch male are activated in situations which arouse the animal, for example when the birds are chased around the cage or when they are exposed to a female. These areas, the hyperstriatum accessorium-dorsale (HAD), a part of the medial neo-hyperstriatum (MNH), the lateral neo-hyperstriatum (LNH), and a portion of the caudal archi-neostriatum (ANC), show enhanced 2-[14C]deoxyglucose (2-DG) uptake according to the experimental situation. On the basis of these experiments, we examined whether the activation of the areas is correlated with motor activity and is influenced by different isolation times prior to a 2-DG experiment, where courtship of the male birds is elicited by exposing them to a female zebra finch. For this purpose, we isolated male zebra finches for 1 day, 1 week, or 8 weeks, respectively, before we injected the 2-DG and exposed the birds to a female. During the experiment, besides other activities, the number of song motifs performed by the bird and the frequency of changing perches was recorded. Our experiments demonstrate that there is a weak negative correlation between motor activity and 2-DG uptake, and a positive correlation between isolation time and 2-DG uptake. We suggest that long isolation blocks courtship behavior by some unknown mechanisms, and that the "internal drive" of the animal, which possibly corresponds with the activity of the four forebrain areas, is enhanced by isolation and by the fact that the birds do not perform the consummatory behavior. Our results also demonstrate that the 2-DG method can show up small differences in the internal state of an animal, which cannot easily be detected by behavioral measurements.     

Dissociation between extension of the sensitive period for avian vocal learning and dendritic spine loss in the song nucleus lMAN

Several instances of early learning coincide with significant rearrangements of neural connections in regions contributing to these behaviors. In fact developmentally restricted learning may be constrained temporally by the opportunity for experience to selectively maintain appropriate synapses amidst the elimination of exuberant connections. Consistent with this notion, during the normal sensitive period for vocal learning in zebra finches (Taenopygia guttata), there is a decline in the density of dendritic spines within a region essential for song development, the lateral magnocellular nucleus of the anterior nidopallium (lMAN). Moreover, in birds isolated from conspecific song shortly after hatching, both the closure of the sensitive period for vocal learning and the pruning of spines from lMAN neurons is delayed. Here, we employed a more subtle form of deprivation to delay the close of the sensitive period for song learning, and found that late song learning occurred without obvious alterations in the pruning of dendritic spines on lMAN neurons. At posthatch day (PHD) 65 (beyond the end of the normal sensitive period for song memorization in zebra finches), birds isolated from song beginning on PHD30 did not differ from normally reared birds in measures of dendritic spine density on Golgi-Cox stained lMAN neurons. Moreover, tutor exposure from PHD65 to 90 did not increase spine elimination in these isolates (who memorized new song material) relative to controls (who did not). Thus, we conclude that the extent of normally occurring lMAN spine loss is not sufficient to account for the timing of the sensitive period for zebra finch song learning.     

Significance of visual cues in choice behavior in the female zebra finch (<Emphasis Type="Italic">Taeniopygia guttata</Emphasis><Emphasis Type="Italic">castanotis</Emphasis>)

Female zebra finches show a preference for male zebra finches over heterospecific males based solely on the auditory cues of males, such as songs. The present study was designed to investigate whether females show a similar preference for male zebra finches based solely on visual cues. Using a Y-maze apparatus, social preference of female zebra finches was studied between male zebra finches and male Bengalese finches in three experiments. In experiment 1, where female zebra finches could see and hear live male zebra finches and male Bengalese finches, the females preferred to associate with the male zebra finches. In experiment 2, using a sound-attenuated experimental apparatus, subjects could see, but not hear, male zebra finches and male Bengalese finches. The subjects did not show a significant preference for associating with zebra finches. In experiment 3, as in experiment 2, females could see live male zebra finches and male Bengalese finches in the sound-attenuated chambers. However, in experiment 3, the subjects also heard prerecorded auditory cues (i.e., songs and calls) of male zebra finches, which were presented simultaneously in both arms of the maze. Although the females could not use the auditory cues to identify the location of the male zebra finches, they preferred to associate with the male zebra finches rather than the male Bengalese finches. These results suggest that visual cues alone were effective in initiating choice behaviors by females and that auditory cues facilitate such visually based choice behaviors. Electronic Publication     

Social learning of food types in zebra finches (<Emphasis Type="Italic">Taenopygia guttata</Emphasis>) is directed by demonstrator sex and feeding activity

In this study we examined how social learning of feeding preferences by zebra finches was affected by the identity of different demonstrators. We presented adult zebra finches with two demonstrators, one male and one female, that exhibited different food choices, and we recorded their subsequent preference when given a choice between the two food types. Previously it was found that young zebra finches' patterns of social learning are affected by the sex of the individual demonstrating a feeding behaviour. This result could be explained by the lack of exposure these animals had to the opposite sex, or by their mating status. Therefore, we investigated the social learning preferences of adult mated zebra finches. We found the same pattern of directed social learning of a different type of feeding behaviour (food colour): female zebra finches preferred the colour of food eaten by male demonstrators, whereas male zebra finches showed little evidence of any preference for the colour of food eaten by female demonstrators. Furthermore, we found that female observers' preferences were biased by demonstrators' relative feeding activity: the female demonstrator was only ever preferred if it ate less than its male counterpart. Electronic Publication     

Social interaction with siblings is necessary for visual imprinting of species-specific maternal preferences in ducklings (Anas platyrhynchos)

This study was conducted to examine the influence of various social rearing experiences on the development of imprinted visual maternal preferences in domestic mallard ducklings (Anas platyrhynchos) during the first 3 days of postnatal life. Twenty-four-hour-old ducklings were allowed to follow a stuffed mallard hen for 30 min. This experience resulted in a visual preference for the familiar mallard hen over an unfamiliar stuffed redhead (Aythya americana) hen in simultaneous choice tests at 48 hr and 72 hr only if the ducklings were reared in conditions allowing unrestricted social interaction with siblings, as would normally occur in nature. No visual preference for the familiar mallard model was found at 48 hr or at 72 hr if ducklings were reared in social isolation but allowed to see another duckling, reared with one duckling, or reared in a group of ducklings but denied the opportunity for direct social interaction. These results demonstrate the importance of normal social experience in the development of the visual imprinting of filial behavior in ducklings. Imprinting studies have traditionally employed isolation rearing and ignored the precocial bird's natural social context. Thus, the present findings raise doubts about the appropriateness of the usual methods of studying imprinting in the laboratory for an understanding of the process of filial imprinting in nature.     

Vaginal scent marking: effects on ultrasonic calling and attraction of male golden hamsters

Male hamsters were tested for their responses to areas that had been scent marked by intact or vaginectomized females to determine the effects of naturally deposited vaginal secretions on male behavior. In the first experiment males produced more ultrasonic courtship calls when investigating areas marked by intact females than areas scented by vaginectomized females, demonstrating that vaginal marks facilitate such calling. In a wind-tunnel preference test situation in which scent-marked alleys and clean alleys served as sources of odor, males approached the scented alley first if it had been freshly marked by intact females but not if it had been scented by vaginectomized females or other males. Thus, the odors of vaginal marks are sufficient to attract males over short distances. After males entered these alleys they showed a preference for odors of both intact and vaginectomized females over no odors, but still spent significantly more time investigating the odors of intact females than those of vaginectomized females. These experiments indicate that vaginal secretions are one of the primary cues that elicit male courtship calling, and the small quantities of vaginal secretions deposited by females in vaginal marks are sufficient to elicit ultrasonic calling and attract males over short distances. Thus it is likely that vaginal scent marking and ultrasonic calling by females interact to facilitate attraction and location of mates during courtship.     

Auditory basis of maternal attachment in ducklings (Anas platyrhynchos) under simulated naturalistic imprinting conditions

The presence of broodmates during the imprinting process results in peer imprinting that interrupts a visually mediated maternal attachment. We sought to determine the conditions in which group-trained mallard ducklings (Anas platyrhynchos) acquire a maternal attachment. At 48 hr of age, ducklings were allowed to follow a vocal, stuffed mallard hen individually or in groups of 4. Individual ducklings showed a preference for the silent, familiar mallard over an unfamiliar pintail. Ducklings trained in groups did not show a preference. When the mallard maternal call was present during testing, group-trained ducklings overwhelmingly responded to it regardless of whether it came from the familiar mallard or an unfamiliar pintail. Training ducklings in groups, which simulates the natural social context of imprinting, results in peer imprinting. Thus, early in development the young become visually imprinted to each other, and the maternal call mediates attachment to the mother.     

Sexual dimorphism of auditory activity in the zebra finch song system

While the tracheosyringeal motor neurons of anesthetized male zebra finches fire in response to acoustic stimuli, the same motor neurons in females show no such response. Females masculinized by estradiol implants on Days 1 or 2 after hatching may develop auditory responses in their tracheosyringeal motor neurons; the presence of the response is directly related to the degree of masculinization of the estradiol-treated females' telencephalic song centers. In male zebra finches, neurons in HVc (Hyperstriatum Ventrale pars caudalis) respond to sound, and the HVc is necessary for the tracheosyringeal auditory response. Multiunit auditory activity was demonstrated in the HVc of female zebra finches. A single 20-microA pulse delivered to the male HVc elicits a large volley in the tracheosyringeal nerve; microstimulating the female HVc does not evoke a response in the motor nerve. This failure of both auditory and HVc stimulation to elicit a response in the female tracheosyringeal nerve is attributed to the lack of a functional HVc-nucleus Robustus Archistriatalis projection in females. If, as has been suggested, the tracheosyringeal auditory response may be important for the processing of song, female zebra finches might not process song in the same manner as do males.     

Imprinting, Conditioning, and Within-event Learning

Three experiments investigated whether or not the temporal relationship between the visual (V) and auditory (A) components of an imprinting stimulus influenced the acquisition of a visual preference in domestic chicks (Gallus gallus domesticus). In Experiments 1a and 1b, chicks given simultaneous presentations of V and A showed a more marked tendency to approach V than those given sequential exposure to V and A. In Experiments 2 and 3, chicks received exposure to two visual stimuli, V1 and V2. During training, presentations of V1 preceded, followed, or were separated by 30 sec from presentations of a simultaneous compound comprising V2 and A. Chicks in each condition subsequently showed an equivalent preference to approach V2 rather than V1. These results show that filial imprinting, unlike Pavlovian conditioning but like within-event learning, proceeds most readily when training involves the simultaneous presentation of stimuli.     

Social dynamics of group courtship behavior in male red-sided garter snakes (Thamnophis sirtalis parietalis)

Mating in red-sided garter snakes is characterized by the formation of mating balls. Up to 100 males simultaneously court single females. The social dynamics of the formation of these mating balls was examined to determine whether the mating balls are formed simply because of a common attraction to the female or whether males are stimulated by the mating balls themselves. A sexually attractive female garter snake appears to be even more attractive to a male when she is being courted by other males than when she is alone. Male garter snakes courted females more actively when other males were also courting the female than when they were alone with her. There is a positive correlation between the number of additional males present and the amount of courtship activity shown by the test male toward the stimulus female. The extent to which the courtship activity of the test males was stimulated by the presence of additional courting males was not influenced by how actively the additional males courted.     

Interactive and vicarious acquisition of auditory preferences in Northern bobwhite (Colinus virginianus) chicks

Studies examining the effects of stimulus contingency on filial imprinting have produced inconsistent findings. In the current study, day-old bobwhite chicks (Colinus virginianus) received individual 5-min sessions in which they were provided contingent, noncontingent, or vicarious exposure to a variant of a bobwhite maternal assembly call. Chicks given contingent exposure to the call showed a significant preference for the familiar call 24 hr following exposure and significantly greater preferences than chicks given noncontingent exposure. Chicks given vicarious exposure to recordings of another chick interacting with the maternal call showed significant deviations from chance responding; however, the direction of chick preference (toward the familiar or unfamiliar) depended on the particular call used. These results indicate that both direct and indirect (vicarious) exposure to stimulus contingency can enhance the acquisition of auditory preferences in precocial avian hatchlings. Precocial avian hatchlings thus likely play a more active role in directing their own perceptual and behavioral development than has typically been thought.     

Changes in stereotyped central motor patterns controlling vocalization are induced by peripheral nerve injury.

Adult male zebra finches (Taeniopygia guttata), as closed-ended learners, normally crystallize their songs at 90 days of age, and the song remains fixed throughout life (Price, 1979). We show that injuring the tracheosyringeal nerve(s) (each of which innervates the ipsilateral half of the syrinx, the avian vocal organ) results in a short-term deficit in the syllables forming adult male song; this deficit disappears after ts nerve regeneration. However, when adult males were followed for a period of several weeks after unilateral tracheosyringeal nerve injury, long-term changes occurred in the temporal patterning of song. Syllables were deleted, remaining portions of the song were linked, and new syllables were added. Syllables with call-like morphology were less likely to be deleted from and more likely to be added to the song. Deletions were most often contiguous chunks of syllables. Changes in the temporal patterning of song occurred during specific periods following nerve injury, were completed within 100 days after nerve transection, and were not dependent upon regeneration of the ts nerve. The resulting newly formed song patterns were stable, remaining unchanged up to 1 year later. The ability of adult male zebra finches to make specific types of changes to crystallized song indicates that some form of vocal plasticity remains even after song learning is completed, though this plasticity may be restricted to a subset of song characteristics. The limitations on the types of changes that are possible may reflect how song is centrally organized.     

Perception of warble song in budgerigars (Melopsittacus undulatus): evidence for special processing

The long, rambling warble song of male budgerigars is composed of a large number of acoustically complex elements uttered in streams lasting minutes a time and accompanied by various courtship behaviors. Warble song has no obvious sequential structure or patterned repetition of elements, raising questions as to which aspects of it are perceptually salient, whether budgerigars can detect changes in natural warble streams, and to what extent these capabilities are species-specific. Using operant conditioning and a psychophysical paradigm, we examined the sensitivity of budgerigars, canaries, and zebra finches to changes in long (>6?min) natural warble sequences of a male budgerigar. All three species could detect a single insertion of pure tones, zebra finch song syllables, budgerigar contact calls, or warble elements from another budgerigar’s warble. In each case, budgerigars were more sensitive to these changes than were canaries or finches. When warble elements from the ongoing warble stream were used as targets and inserted, out of order, into the natural warble stream so that the only cue available was the violation of the natural ordering of warble elements, only budgerigars performed above chance. When the experiment was repeated with all the ongoing warble stream elements presented in random order, the performance of budgerigars fell to chance. These results show species-specific advantages in budgerigars for detecting acoustic changes in natural warble sequences and indicate at least a limited sensitivity to sequential rules governing the structure of their species-specific warble songs.     

Chicks like consonant music

The question of whether preference for consonance is rooted in acoustic properties important to the auditory system or is acquired through enculturation has not yet been resolved. Two-month-old infants prefer consonant over dissonant intervals, but it is possible that this preference is rapidly acquired through exposure to music soon after birth or in utero. Controlled-rearing studies with animals can help shed light on this question because such studies allow researchers to distinguish between biological predispositions and learned preferences. In the research reported here, we found that newly hatched domestic chicks show a spontaneous preference for a visual imprinting object associated with consonant sound intervals over an identical object associated with dissonant sound intervals. We propose that preference for harmonic relationships between frequency components may be related to the prominence of harmonic spectra in biological sounds in natural environments.     

A framework for the study of filial imprinting and the development of attachment

Filial imprinting is the process through which early attachment behavior becomes restricted to the mother and siblings. In the present paper it will be shown that the processes underlying imprinting in chicks (Gallus gallus) can be fruitfully analyzed by referring to the same mechanisms as are generally assumed to play a role in perceptual and associative learning. This can be achieved within a framework formulated to study the development of behavior in general. This offers the opportunity to apply the same general framework to the study of filial imprinting and the further development of attachment. The involvement of perceptual and associative processes in imprinting is discussed in some detail, while the broader implications of the present approach are indicated only briefly.     

Song recognition in zebra finches: Are there sensitive periods for song memorization?

Male zebra finches learn to sing songs that they hear between 25 and 65 days of age, the sensitive period for song learning. In this experiment, male and female zebra finches were exposed to zebra finch songs either before (n = 9) or during (n = 4) the sensitive period. Following song exposure, recognition memory for the songs was assessed with an operant discrimination between familiar and novel songs. Zebra finches that were exposed to songs between 22 and 30 days of age discriminated between familiar and novel songs; zebra finches exposed to songs from 9 to 17 days of age did not. Failure to memorize songs heard prior to the sensitive period may contribute to the exclusion of those songs from the repertoire of songbirds.     

Avoidance of relatively aggressive male Japanese Quail (Coturnix japonica) by sexually experienced conspecific females

Sexually experienced female Japanese quail (Coturnix japonica) that are offered a choice between 2 conspecific males previously observed engaging in an aggressive encounter prefer to affiliate with the less aggressive male. The authors determined whether this apparent preference for less aggressive males results from females approaching less aggressive individuals or avoiding more aggressive individuals. The authors found that females that had seen 2 males fight before choosing, in counterbalanced order, between each of them and a neutral stimulus were indifferent to less aggressive males but avoided more aggressive males. The results are consistent with the view that in species in which male courtship and mating are potentially harmful to females, females keep away from relatively aggressive males in order to avoid the physical punishment that can result from contact with them.     

Courtship learning in Drosophila melanogaster: Diverse plasticity of a reproductive behavior

Mechanisms for identifying appropriate mating partners are critical for species propagation. In many species, the male uses multiple sensory modalities to search for females and to subsequently determine if they are fit and receptive. Males can also use the information they acquire in this process to change their courtship behavior and reduce courtship of classes of targets that are inappropriate or unreceptive. In Drosophila, courtship plasticity, in the form of both nonassociative and associative learning, has been documented—the type of learning depending on the nature of the trainer. The conditions in which the male is presented with the training target can profoundly alter the cues that he finds salient and the longevity of the memory that he forms. With the exception of habituation and sensitization, these types of plasticity have an operant component in that the male must be courting to respond to the behavior-altering cues. Courtship plasticity is therefore a complex and rich range of behaviors rather than a single entity. Our understanding of these plastic behaviors has been enhanced by recent advances in our understanding of the circuitry underlying courtship itself and the identification of chemical cues that drive and modify the behavior. Courtship learning is providing a window into how animals can use a variety of sensory inputs to modulate a decision making process at many levels.When confronted with a potential mate, Drosophila melanogaster males perform a stereotyped courtship ritual. This behavior serves at least two obvious functions for the male. The first is to prime conspecific females for copulation. During courtship, the female is assessing the male''s suitability, and if the song he sings (Burnet et al. 1971; von Schilcher 1976a) and pheromones he emits (Grillet et al. 2006; Kurtovic et al. 2007) are correct for her species and of sufficient quality, her willingness to copulate is increased. She will slow her locomotion, present her abdomen to the male, and then spread her wings and genital plates to allow him to mount (Lasbleiz et al. 2006). A second function of courtship is that it allows a male to accumulate information about the target courtship object to assess its suitability and receptiveness. The male uses auditory, mechanosensory, visual, and chemosensory signals from the target to make this assessment (for review, see Villella and Hall 2008; Ejima and Griffith 2009).Since D. melanogaster males will avidly initiate courtship of a wide variety of inappropriate and/or unreceptive targets, including immature males, sexually immature virgin females, mated females, and heterospecific females, the information obtained during courtship is critical to deciding whether to increase the intensity of his effort or terminate pursuit of the target. In the last several years, courtship has become a favored model for those researchers interested in how the nervous system specifies “innate” behaviors. While it is true that a male does not have to be instructed to produce adequate courtship (Hall 1994; Clyne and Miesenbock 2008), this apparently stereotyped behavior is far from static: It can be modified in a dizzying number of ways by experience. In this paper, we will discuss how information gathered during courtship can allow males to learn about specific types of courtship objects and broadly modify future behavioral responses to a particular class of target.     

Effect of acoustic cue modifications on evoked vocal response to calls in zebra finches (Taeniopygia guttata)

Besides their song, which is usually a functionally well-defined communication signal with an elaborate acoustic structure, songbirds also produce a variety of shorter vocalizations named calls. While a considerable amount of work has focused on information coding in songs, little is known about how calls' acoustic structure supports communication processes. Because male and female zebra finches use calls during most of their interactions and answer to conspecific calls without visual contact, we aimed at identifying which calls' acoustic cues are necessary to elicit a vocal response. Using synthetic zebra finch calls, we examined evoked vocal response of male and female zebra finches to modified versions of the distance calls. Our results show that the vocal response of zebra finches to female calls requires the full harmonic structure of the call, whereas the frequency downsweep of male calls is necessary to evoke a vocal response. It is likely that both female and male calls require matching a similar frequency bandwidth to trigger a response in conspecific individuals.     

Responsivity to pain in rats changed by the ingestion of flavored water

Sprague-Dawley male rats drank flavored water and subsequent pain responsivity was assessed using a hot plate first after isotonic saline and later after either 2.75 (Experiment 1) or 2.5 (Experiment 2) mg/kg of morphine hydrochloride was injected. A 48-h exposure to any one of several different flavors resulted in a reduction of the analgesic effects of morphine as shown by an attenuation of the increased latency to paw lick caused by the morphine. This effect was independent of the amount consumed. A 26-h exposure to a flavor decreased pain reactivity before and after morphine as shown by an overall increase in latency to paw lick. This effect was not influenced by whether the normally preferred flavor was made aversive by a previous pairing with lithium chloride-induced illness. These findings are consistent with the idea that many flavors, independently of palatability and amount consumed, increase the release and utilization of endogenous opioids.