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The sexually dimorphic robust archistriatal nucleus (RA) represents the telencephalic output of the bird song system. Here, we document sex-dependent changes in both the metabolic and neuronal activity of RA during the sensory and sensorimotor phases of song learning. From posthatching day (PHD) 20-63 in males but not females, RA and its input nucleus HVc showed sharp increases in cytochrome oxidase (CO) activity relative to surrounding archistriatum and the underlying shelf, respectively. In urethane-anesthetized birds, during the same period, the spontaneous activity of male RA neurons underwent dramatic changes in firing rate, distribution of interspike intervals, and bursting frequency, compared with other archistriatal cells. At PHD 20-21, RA neurons had extremely slow, irregular firing rates in birds of both sexes. In males, from PHD 30-36, RA neurons increased their firing rates and spiking activity became more regular, and at approximately PHD 38, strong bursts followed by inhibition (which in awake animals is associated with singing) began to be observed. Dual recordings from RA and HVc revealed synchronous bursting, with RA spikes lagging approximately 10 msec behind HVc. We conclude that changes in relative CO activity correlate with changes in spontaneous firing rates within RA and that patterns of RA spontaneous activity exhibit gradual change as birds enter early song and then again for plastic song. The emergence of strong burst patterns in RA occurs later in life than does input from HVc as established by tracer studies or based on observed HVc bursting in young animals.

We explored physiological changes correlated with song tutoring by recording the responses of caudal nidopallium neurons of zebra finches aged P21-P24 (days post hatching) to a broad spectrum of natural and synthetic stimuli. Those birds raised with their fathers tended to show behavioral evidence of song memorization but not of singing; thus auditory responses were not confounded by the birds' own vocalizations. In study 1, 37 of 158 neurons (23%) in 17 of 22 tutored and untutored birds were selective for only 1 of 10 stimuli comprising broadband signals, early juvenile songs and calls, female calls, and adult songs. Approximately 30% of the selective neurons (12/37 neurons in 9 birds) were selective for adult conspecific songs. All these were found in the song system nuclei HVC and paraHVC. Of 122 neurons (17 birds) in tutored birds, all of the conspecific song-selective neurons (8 neurons in 6 birds) were selective for the adult tutor song; none was selective for unfamiliar song. In study 2 with a different sampling strategy, we found that 11 of 12 song-selective neurons in 6 of 7 birds preferred the tutor song; none preferred unfamiliar or familiar conspecific songs. Most of these neurons were found in caudal lateral nidopallium (NCL) below HVC. Thus by the time a bird begins to sing, there are small numbers of tutor song-selective neurons distributed in several forebrain regions. We hypothesize that a small population of higher-order auditory neurons is innately selective for complex features of behaviorally relevant stimuli and these responses are modified by specific perceptual/social experience during development.

Simple SummaryTiti monkeys—a diversified group of pair-bonded, territorial neotropical primates exhibiting biparental care—produce elaborate, powerful vocal duets used for long-range communication. While the callicebine taxonomy has been centered mainly on the biogeography, morphology, anatomy, and genetics of titi populations, vocal attributes have received little attention as potentially informative markers of phylogenetic relationships. We conducted acoustic analysis of callicebine loud calls recorded from ten species of titis at sites in Bolivia, Peru, and Ecuador and found four distinct patterns of duetting that only partially match three major clades identified in recent molecular genetic studies. In particular, we found that the loud calls of the San Martin titi monkey, P. oenanthe, and the Urubamba brown titi, P. urubambensis, strikingly differ from putative relatives within the donacophilus lineage. Our findings highlight interplay between genes and environment on the expression of vocal behavior and suggest that closer interaction between taxonomists, ethologists, and molecular biologists should be rewarding in resolving the callicebine phylogeny. Such concerted efforts, in turn, will most likely generate valuable recommendations for the conservation of some endangered populations of titi monkeys, such as the vocally distinctive San Martin titi.AbstractLong-range vocal communication in socially monogamous titi monkeys is mediated by the production of loud, advertising calls in the form of solos, duets, and choruses. We conducted a power spectral analysis of duets and choruses (simply “duets” hereafter) followed by linear discriminant analysis using three acoustic parameters—dominant frequency of the combined signal, duet sequence duration, and pant call rate—comparing the coordinated vocalizations recorded from 36 family groups at 18 sites in Bolivia, Peru and Ecuador. Our analysis identified four distinct duetting patterns: (1) a donacophilus pattern, sensu stricto, characteristic of P. donacophilus, P. pallescens, P. olallae, and P. modestus; (2) a moloch pattern comprising P. discolor, P. toppini, P. aureipalatii, and P. urubambensis; (3) a torquatus pattern exemplified by the duet of Cheracebus lucifer; and (4) the distinctive duet of P. oenanthe, a putative member of the donacophilus group, which is characterized by a mix of broadband and narrowband syllables, many of which are unique to this species. We also document a sex-related difference in the bellow-pant phrase combination among the three taxa sampled from the moloch lineage. Our data reveal a presumptive taxonomic incoherence illustrated by the distinctive loud calls of both P. urubambensis and P. oenanthe within the donacophilus lineage, sensu largo. The results are discussed in light of recent reassessments of the callicebine phylogeny, based on a suite of genetic studies, and the potential contribution of environmental influences, including habitat acoustics and social learning. A better knowledge of callicebine loud calls may also impac...

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