Responses to song playback differ in sleeping versus anesthetized songbirds

Vocal learning in songbirds is mediated by a highly localized system of interconnected forebrain regions, including recurrent loops that traverse the cortex, basal ganglia, and thalamus. This brain-behavior system provides a powerful model for elucidating mechanisms of vocal learning, with implications for learning speech in human infants, as well as for advancing our understanding of skill learning in general. A long history of experiments in this area has tested neural responses to playback of different song stimuli in anesthetized birds at different stages of vocal development. These studies have demonstrated selectivity for different song types that provide neural signatures of learning. In contrast to the ease of obtaining responses to song playback in anesthetized birds, song-evoked responses in awake birds are greatly reduced or absent, indicating that behavioral state is an important determinant of neural responsivity. Song-evoked responses can be elicited in sleeping as well as anesthetized zebra finches, and the selectivity of responses to song playback in adult birds tends to be highly similar between anesthetized and sleeping states, encouraging the idea that anesthesia and sleep are highly similar. In contrast to that idea, we report evidence that cortical responses to song playback in juvenile zebra finches (Taeniopygia guttata) differ greatly between sleep and urethane anesthesia. This finding indicates that behavioral states differ in sleep versus anesthesia and raises questions about relationships between developmental changes in sleep activity, selectivity for different song types, and the neural substrate for vocal learning.

Response Properties of Optic Flow Neurons in the Accessory Optic System of Hummingbirds vs. Zebra Finches and Pigeons

Optokinetic responses function to maintain retinal image stabilization by minimizing optic flow that occurs during self-motion. The hovering ability of hummingbirds is an extreme example of this behaviour. Optokinetic responses are mediated by direction-selective neurons with large receptive fields in the accessory optic system (AOS) and pretectum. Recent studies in hummingbirds showed that, compared to other bird species, (i) the pretectal nucleus lentiformis mesencephali (LM) is hypertrophied, (ii) LM has a unique distribution of direction preferences, and (iii) LM neurons are more tightly tuned to stimulus velocity. In this study, we sought to determine if there are concomitant changes in the nucleus of the basal optic root (nBOR) of the AOS. We recorded the visual response properties of nBOR neurons to largefield drifting random dot patterns and sine wave gratings in Anna's hummingbirds and zebra finches and compared these with archival data from pigeons. We found no differences with respect to the distribution of direction preferences: Neurons responsive to upwards, downwards and nasal-to-temporal motion were equally represented in all three species, and neurons responsive to temporal-to-nasal motion were rare or absent (<5%). Compared to zebra finches and pigeons, however, hummingbird nBOR neurons were more tightly tuned to stimulus velocity of random dot stimuli. Moreover, in response to drifting gratings, hummingbird nBOR neurons are more tightly tuned in the spatio-temporal domain. These results, in combination with specialization in LM, supports a hypothesis that hummingbirds have evolved to be "optic flow specialist" to cope with the optomotor demands of sustained hovering flight.

Born without night: The consequence of the no-night environment on reproductive performance in diurnal zebra finches

We investigated the consequence of no night environment (constant light, LL) on reproductive performance in zebra finches in the parent (P) and subsequent F1 generation. As a measure of the overall effects on the metabolic reproductive health, we monitored daily activity behaviour, recorded song and cheek patch size in males, and measured body size and hormone levels. As compared to controls under 12 h light: 12 h darkness (12:12 h LD), both P and F1 pairs showed a compromised reproductive success, as evidenced by fewer fledglings and viable offsprings with longer fledging durations, and increased offspring mortality with successive three clutches under LL. The overall negative effect of the no-night environment was increased in the F1generation. As compared to P pairs, F1pairs had more failed nesting and breeding attempts, took longer to initiate reproduction, incubated fewer eggs, produced fewer viable offspring with longer fledging duration, and showed increased offspring mortality. Consistent with negative reproductive effects, P males showed significant changes in the motif duration and other spectral features of song, and both F1 and F2 males copied poorly the song of their parent under LL. Plasma corticosterone and sex hormones (testosterone in males and estradiol in females) levels were significantly lower under LL. Daily plasma melatonin rhythm persisted but with a reduced amplitude under LL. These results demonstrate the importance of night in reproduction in a continuously breeding diurnal species, and give insights into the possible impact on physiology of animals whose surrounding environment is consistently losing the darkness of night.

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.

Effects of Night Illumination on Behavior, Body Mass and Learning in Male Zebra Finches

An increase in artificial night lighting has blurred the boundaries of day and night and transformed the natural day-night environment with alteration in the temporal niche of the animals. Male zebra finches were exposed to a dim light at night (dLAN) protocol (Light: dLAN, 12L = 200 lux: 12dLAN = 5 lux) with controls on darkness at night (Light: dark, 12L = 200 lux: 12D = 0 lux) for six weeks. We assayed sleep-wake, daily behaviors, mood, and cognition, as well as changes in physiological parameters. Dim light at night increased sleep frequency, delayed sleep onset, advanced awakening latency, and caused a reduction in total sleep duration. dLAN birds did not associate (physical association) with novel object and birds spent significantly lesser time on perch with novel object as compared to LD. In colour learning task, night illuminated birds took more time to learn and made more error, compared to LD. dLAN significantly altered the 24-h daily behavioral rhythm (amplitude and acrophase) of feeding, drinking, preening, and perch-hopping behavior. In particular, birds extended their feeding hours in the nighttime under dLAN, with no difference in total food intake. Birds under dLAN increased fattening and hence significantly increased body mass. Our results show that dim light at night altered feeding rhythm, caused decrease in sleep behavior, and negatively affected learning and memory performance in male zebra finches.

Intrinsic motivation for singing in songbirds is enhanced by temporary singing suppression and regulated by dopamine

Behaviors driven by intrinsic motivation are critical for development and optimization of physical and brain functions, but their underlying mechanisms are not well studied due to the complexity and autonomy of the behavior. Songbirds, such as zebra finches, offer a unique opportunity to study neural substrates of intrinsic motivation because they spontaneously produce many renditions of songs with highly-quantifiable structure for vocal practice, even in the absence of apparent recipients (“undirected singing”). Neural substrates underlying intrinsic motivation for undirected singing are still poorly understood partly because singing motivation cannot be easily manipulated due to its autonomy. Also, undirected singing itself acts as an internal reward, which could increase singing motivation, leading to difficulty in measuring singing motivation independent of singing-associated reward. Here, we report a simple procedure to easily manipulate and quantify intrinsic motivation for undirected singing independent of singing-associated reward. We demonstrate that intrinsic motivation for undirected singing is dramatically enhanced by temporary suppression of singing behavior and the degree of enhancement depends on the duration of suppression. Moreover, by examining latencies to the first song following singing suppression as a measure of singing motivation independent of singing-associated reward, we demonstrate that intrinsic singing motivation is critically regulated by dopamine through D2 receptors. These results provide a simple experimental tool to manipulate and measure the intrinsic motivation for undirected singing and illustrate the importance of zebra finches as a model system to study the neural basis of intrinsically-motivated behaviors.