Carolyn L. Pytte

How sleep affects the developmental learning of bird song.

Sleep affects learning and development in humans and other animals, but the role of sleep in developmental learning has never been examined. Here we show the effects of night-sleep on song development in the zebra finch by recording and analysing the entire song ontogeny. During periods of rapid learning we observed a pronounced deterioration in song structure after night-sleep. The song regained structure after intense morning singing. Daily improvement in similarity to the tutored song occurred during the late phase of this morning recovery; little further improvement occurred thereafter. Furthermore, birds that showed stronger post-sleep deterioration during development achieved a better final imitation. The effect diminished with age. Our experiments showed that these oscillations were not a result of sleep inertia or lack of practice, indicating the possible involvement of an active process, perhaps neural song-replay during sleep. We suggest that these oscillations correspond to competing demands of plasticity and consolidation during learning, creating repeated opportunities to reshape previously learned motor skills.

Regulation of vocal amplitude by the blue-throated hummingbird, Lampornis clemenciae

Animals that rely on vocal communication must broadcast sound so that a perceptible signal is transmitted over an appropriate distance. We found that male blue-throated hummingbirds modified the amplitude of their vocalizations in response to both naturally occurring and experimenter-controlled changes in ambient noise levels. This phenomenon is known as the Lombard effect and may increase the efficiency of acoustic signalling. This study demonstrates the effect under natural field conditions and documents the first hummingbird species (Apodiformes: Trochilidae) to show this behaviour. We measured sound pressure levels (SPLs) of Serial Chip territorial advertisement calls across a natural range of ambient noise, primarily due to creeks within male territories. We found a significant correlation between the amplitude of Serial Chips and the amplitude of background noise. To test this relationship, we broadcast recordings of creek noise at high and low amplitudes while target individuals were producing Serial Chip vocalizations. We measured vocal SPLs before and during the playback. Individuals responded to changes in playback creek noise by changing the amplitude of Serial Chip production. We also measured transmission properties of Serial Chip calls through natural habitat to calculate the approximate amplitude of vocalizations at the position of the calling bird. We suggest that amplitude regulation of vocalizations contibutes to signal transmission distance along with the established relationships between singing behaviour, acoustic structure and habitat. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.

Sensitive Period for Sensorimotor Integration during Vocal Motor Learning

Sensory experience during sensitive periods in development may direct the organization of neural substrates, thereby permanently influencing subsequent adult behavior. We report a sensitive period during the imitative motor learning phase of sensorimotor integration in birdsong development. By temporarily and reversibly blocking efference to the vocal muscles, we disrupted vocal motor practice during selected stages of song development. Motor disruption during prolonged periods early in development, which allows recovery of vocal control prior to the onset of adult song, has no effect on adult song production. However, song disruption late in development, during the emergence of adult song, results in permanent motor defects in adult song production. These results reveal a decreased ability to compensate for interference with motor function when disturbances occur during the terminal stage of vocal motor development. Temporary disruption of syringeal motor control in adults does not produce permanent changes in song production. Permanent vocal aberrations in juveniles are evident exclusively in learned song elements rather than nonlearned calls, suggesting that the sensitive period is associated with motor learning.

A bird's own song contributes to conspecific song perception.

We investigated the role of developmental vocal experience in adult song perception by muting juvenile male zebra finches prior to song development and testing their behavioral responses to song playback as adults. Birds were raised in a normal social and acoustic environment. Non-treated sibling control birds demonstrated statistically significant phonotactic preferences for particular conspecific familiar or novel songs. Muted birds responded to playbacks at chance levels, showing no preferences for individual conspecific songs. These results suggest that the acquisition of a birds own song may contribute to the perceptual processing, recognition, or discrimination of different conspecific songs.

Adult neurogenesis is associated with the maintenance of a stereotyped, learned motor behavior

Adult neurogenesis is thought to provide neural plasticity used in forming and storing new memories. Here we show a novel relationship between numbers of new neurons and the stability of a previously learned motor pattern. In the adult zebra finch, new projection neurons are added to the nucleus HVC and become part of the motor pathway for producing learned song. However, new song learning occurs only in juveniles and the behavioral impact of adding new neurons to HVC throughout life is unclear. We report that song changes after deafening are inversely correlated with the number of new neurons added to HVC, suggesting that adult neurogenesis in this context may contribute to behavioral stability. More broadly, we propose that new neuron function may depend on the site of integration and can vary as widely as promoting, or restricting, behavioral plasticity.

Nest of Origin Predicts Adult Neuron Addition Rates in the Vocal Control System of the Zebra Finch

Neurogenesis and neuronal replacement in adulthood represent dramatic forms of plasticity that might serve as a substrate for behavioral flexibility. In songbirds, neurons are continually replaced in HVC (used as a proper name), a pre-motor region necessary for the production of learned vocalizations. There are large individual differences in HVC neuron addition. Some of this variation is probably due to individual differences in adult experience; however, it is also possible that heritability or experience early in development constrains the levels of adult neuron addition. As a step toward addressing the latter two possibilities, we explored the extent to which nest of origin predicts rates of HVC neuron addition in adult male zebra finches. One month after injections of [3H]-thymidine to mark dividing cells, neuron addition in HVC was found to co-vary among birds that had been nest mates, even when they were housed in different cages as adults. We also tested whether nest mate co-variation might be due to shared adult auditory experience by measuring neuron addition in nest mate pairs after one member was deafened. There were significant differences in neuron addition between hearing and deaf birds but nest mate relationships persisted. These results suggest that variation in genotype and/or early pre- or postnatal experience can account for a large fraction of adult variation in rates of neuron addition. These results also suggest that a major constraint on neurogenesis and the capacity to adjust rates of neuron addition in response to adult auditory experience is established early in development.

Organization of agonistic vocalizations in Black-chinned Hummingbirds

We describe vocalizations of Black-chinned Hummingbirds (Archilochus al- exandrl) recorded during agonistic encounters at feeders. Calls are composed of one to five different note-types that comprise a recombinatorial system exhibiting syntax. A Markov analysis revealed non-random ordering of note-types. The distribution of call-types (unique combinations of notes) illustrates openness; the number of call-types increases as more calls are sampled. Constraints on call length occur that are related to the length of individual note-types; shorter note-types are more common in calls with more notes. No sex differences occurred in the call-types with the exception of the Z note which occurred more often in male calls. The agonistic vocalizations of these hummingbirds demonstrate a level of vocal complexity comparable to songs of many passeriues. We compare the vocalizations of the Black-chinned Hummingbird with studies ofAnnas Hummingbird (CaZypte anna) and point out major differences in repertoire organization. Marked similarities occur between orga- nization of calls in certain chickadees (Parus) and that of the Black-chinned Hummingbird. This finding is surprising in view of their phyletic differences, but may reflect certain un- derlying constraints on the organization of avian vocalizations.

Adult neuron addition to the zebra finch song motor pathway correlates with the rate and extent of recovery from botox-induced paralysis of the vocal muscles

In adult songbirds, neurons are continually incorporated into the telencephalic nucleus HVC (used as a proper name), a premotor region necessary for the production of learned vocalizations. Previous studies have demonstrated that neuron addition to HVC is highest when song is most variable: in juveniles during song learning, in seasonally singing adults during peaks in plasticity that precede the production of new song components, or during seasonal reestablishment of a previously learned song. These findings suggest that neuron addition provides motor flexibility for the transition from a variable song to a target song. Here we test the association between the quality of song structure and HVC neuron addition by experimentally manipulating syringeal muscle control with Botox, which produces a transient partial paralysis. We show that the quality of song structure covaries with new neuron addition to HVC. Both the magnitude of song distortion and the rate of song recovery after syringeal Botox injections were correlated with the number of new neurons incorporated into HVC. We suggest that the quality of song structure is either a cause or consequence of the number of new neurons added to HVC. Birds with naturally high rates of neuron addition may have had the greatest success in recovering song. Alternatively, or in addition, new neuron survival in the song motor pathway may be regulated by the quality of song-generated feedback as song regains its original stereotyped structure. Present results are the first to show a relationship between peripheral muscle control and adult neuron addition to cortical premotor circuits.

Ventromedial and medial preoptic hypothalamic ibotenic acid lesions potentiate systemic morphine analgesia in female, but not male rats.

Sex differences in systemic morphine analgesia occur with male rodents displaying significantly greater analgesic magnitudes and potencies than females. Neonatal androgenization, and to a lesser degree, adult ovariectomy enhance systemic morphine analgesia in female rats, implicating both organizational and activational effects of gonadal hormones. The neuroanatomical circuits sensitive to sex-related hormones by which females display a smaller opiate analgesic effect is not clear, but the ventromedial (VMH) and medial preoptic (MPOA) hypothalamic nuclei are critical in the monitoring of estradiol and other sex hormone levels. To assess the contribution of these nuclei to sex and adult gonadectomy differences in systemic morphine analgesia, intact male, intact female and adult ovariectomized (OVEX) female rats received bilateral saline (SAL) or ibotenic acid (IBO) microinjections into either the VMH or MPOA. Following surgeries, baseline tail-flick latencies over 120 minutes (min) were assessed over 4 days in all nine groups with intact females tested in the estrus phase of their cycle. All animals then received an ascending series of morphine (1.0, 2.5, 5.0, 7.5, 10.0mg/kg) injections 30min prior to the tail-flick test time course with 8-12 day inter-injection intervals between doses. Baseline latencies failed to differ between SAL-treated intact males and females, but were significantly higher in SAL-treated OVEX females. Both VMH IBO and MPOA IBO lesions increased baseline latencies in intact male and female rats, but not in OVEX females. SAL-treated intact males (ED(50)=4.0mg/kg) and SAL-treated OVEX females (ED(50)=3.5mg/kg) displayed significantly greater potencies of systemic morphine analgesia than SAL-treated intact females (ED(50)=6.3mg/kg), confirming previous gender and gonadectomy differences. Neither VMH IBO (ED(50)=3.7 mg/kg) nor MPOA IBO (ED(50)=4.1mg/kg) males differed from SAL-treated males in the potency of systemic morphine analgesia. In contrast, VMH IBO (ED(50)=4.1mg/kg) and MPOA IBO (ED(50)=3.5mg/kg) intact females displayed significantly greater potencies in systemic morphine analgesia than SAL-treated intact females. However, VMH IBO OVEX (ED(50)=3.5mg/kg) and MPOA IBO OVEX (ED(50)=3.9 mg/kg) failed to differ from SAL-treated OVEX females in the potency of systemic morphine analgesia. The magnitudes of systemic morphine analgesia as measured by Maximum Percentage Effect values displayed similar patterns, but lesser degrees, of effects. These data suggest that VMH and MPOA nuclei act to tonically inhibit endogenous pain-inhibitory circuits in the intact female, but not intact male brain, and that removal of circulating gonadal hormones by OVEX and/or excitotoxic destruction of these estrogen receptor accumulating nuclei disinhibit the female analgesic response to systemic morphine.

Deafening decreases neuronal incorporation in the zebra finch caudomedial nidopallium (NCM)

New neurons formed in the adult brain are incorporated into existing circuits. However, the number of new neurons recruited into a given brain region varies widely depending on the experience of the animal. An emerging general principle is that recruitment and early neuronal survival may be correlated with activity or use of the brain region. Here we show that use-dependent neuronal survival also occurs in the higher order auditory processing region of the songbird caudomedial nidopallium (NCM). We suggest that retention of young neurons may in part be influenced by use of the system without an increased demand for learning or behavioral plasticity.