Recovery of hearing and vocal behavior after hair-cell regeneration

Postmitotic hair-cell regeneration in the inner ear of birds provides an opportunity to study the effect of renewed auditory input on auditory perception, vocal production, and vocal learning in a vertebrate. We used behavioral conditioning to test both perception and vocal production in a small Australian parrot, the budgerigar. Results show that both auditory perception and vocal production are disrupted when hair cells are damaged or lost but that these behaviors return to near normal over time. Precision in vocal production completely recovers well before recovery of full auditory function. These results may have particular relevance for understanding the relation between hearing loss and human speech production especially where there is consideration of an auditory prosthetic device. The present results show, at least for a bird, that even limited recovery of auditory input soon after deafening can support full recovery of vocal precision.

Discovery of genes involved with learning and memory: An experimental synthesis of Hirschian and Benzerian perspectives

The biological bases of learning and memory are being revealed today with a wide array of molecular approaches, most of which entail the analysis of dysfunction produced by gene disruptions. This perspective derives both from early “genetic dissections” of learning in mutant Drosophila by Seymour Benzer and colleagues and from earlier behavior-genetic analyses of learning and in Diptera by Jerry Hirsch and coworkers. Three quantitative-genetic insights derived from these latter studies serve as guiding principles for the former. First, interacting polygenes underlie complex traits. Consequently, learning/memory defects associated with single-gene mutants can be quantified accurately only in equilibrated, heterogeneous genetic backgrounds. Second, complex behavioral responses will be composed of genetically distinct functional components. Thus, genetic dissection of complex traits into specific biobehavioral properties is likely. Finally, disruptions of genes involved with learning/memory are likely to have pleiotropic effects. As a result, task-relevant sensorimotor responses required for normal learning must be assessed carefully to interpret performance in learning/memory experiments. In addition, more specific conclusions will be obtained from reverse-genetic experiments, in which gene disruptions are restricted in time and/or space.

Song selectivity and sensorimotor signals in vocal learning and production

Bird song, like human speech, is a learned vocal behavior that requires auditory feedback. Both as juveniles, while they learn to sing, and as adults, songbirds use auditory feedback to compare their own vocalizations with an internal model of a target song. Here we describe experiments that explore a role for the songbird anterior forebrain pathway (AFP), a basal ganglia-forebrain circuit, in evaluating song feedback and modifying vocal output. First, neural recordings in anesthetized, juvenile birds show that single AFP neurons are specialized to process the song stimuli that are compared during sensorimotor learning. AFP neurons are tuned to both the bird's own song and the tutor song, even when these stimuli are manipulated to be very different from each other. Second, behavioral experiments in adult birds demonstrate that lesions to the AFP block the deterioration of song that normally follows deafening. This observation suggests that deafening results in an instructive signal, indicating a mismatch between feedback and the internal song model, and that the AFP is involved in generating or transmitting this instructive signal. Finally, neural recordings from behaving birds reveal robust singing-related activity in the AFP. This activity is likely to originate from premotor areas and could be modulated by auditory feedback of the bird's own voice. One possibility is that this activity represents an efference copy, predicting the sensory consequences of motor commands. Overall, these studies illustrate that sensory and motor processes are highly interrelated in this circuit devoted to vocal learning, as is true for brain areas involved in speech.

Neural systems underlying learning and representation of global motion

We demonstrate performance-related changes in cortical and cerebellar activity. The largest learning-dependent changes were observed in the anterior lateral cerebellum, where the extent and intensity of activation correlated inversely with psychophysical performance. After learning had occurred (a few minutes), the cerebellar activation almost disappeared; however, it was restored when the subjects were presented with a novel, untrained direction of motion for which psychophysical performance also reverted to chance level. Similar reductions in the extent and intensity of brain activations in relation to learning occurred in the superior colliculus, anterior cingulate, and parts of the extrastriate cortex. The motion direction-sensitive middle temporal visual complex was a notable exception, where there was an expansion of the cortical territory activated by the trained stimulus. Together, these results indicate that the learning and representation of visual motion discrimination are mediated by different, but probably interacting, neuronal subsystems.

Phalangeal curvature and positional behavior in extinct sloth lemurs (Primates, Palaeopropithecidae)

Recent paleontological discoveries in Madagascar document the existence of a diverse clade of palaeopropithecids or “sloth lemurs”: Mesopropithecus (three species), Babakotia (one species), Palaeopropithecus (three species), and Archaeoindris (one species). This mini-radiation of now extinct (“subfossil”) lemurs is most closely related to the living indrids (Indri, Propithecus, and Avahi). Whereas the extant indrids are known for their leaping acrobatics, the palaeopropithecids (except perhaps for the poorly known giant Archaeoindris) exhibit numerous skeletal design features for antipronograde or suspensory positional behaviors (e.g., high intermembral indices and mobile joints). Here we analyze the curvature of the proximal phalanges of the hands and feet. Computed as the included angle (θ), phalangeal curvature develops in response to mechanical use and is known to be correlated in primates with hand and foot function in different habitats; terrestrial species have straighter phalanges than their arboreal counterparts, and highly suspensory forms such as the orangutan possess the most curved phalanges. Sloth lemurs as a group are characterized by very curved proximal phalanges, exceeding those seen in spider monkeys and siamangs, and approaching that of orangutans. Indrids have curvatures roughly half that of sloth lemurs, and the more terrestrial, subfossil Archaeolemur possesses the least curved phalanges of all the indroids. Taken together with many other derived aspects of their postcranial anatomy, phalangeal curvature indicates that the sloth lemurs are one of the most suspensory clades of mammals ever to evolve.