Journal Article

Neural mechanisms of birdsong memory

Gahr, Manfred, Bolhuis, Johan J.

2006

Overview

Key Points Song learning in songbirds has strong similarities with speech acquisition in human infants. Songbirds need to learn their songs from an adult conspecific. This occurs in two phases: a memorization phase, early in life, during which the young bird forms a neural representation (a 'template') of the song of a tutor; and a sensorimotor phase, during which the bird's own vocal output is matched to the stored template. A network of interconnected brain nuclei, known as the 'song system', is involved in the perception, learning and production of song. Within the song system, the caudal pathway is important for song production. The rostral pathway is involved in song perception and in vocal sensorimotor learning. Initial claims that there are correlations between functional (for example, seasonal or sex) song differences and differences in song system morphology have not been supported by recent findings. Two regions outside the song system show neuronal activation (measured as increased expression of immediate early genes) when zebra finches are exposed to song. In one of these regions, the caudomedial nidopallium (NCM), neuronal activation on exposure to the tutor song is significantly correlated with the strength of song learning. An electrophysiological study showed that a familiarity index, based on neuronal habituation rates in the NCM, was significantly greater in tutored males than in untutored males, and significantly positively correlated with the strength of song learning. Zebra finch females do not sing, but nevertheless can learn the characteristics of their father's song and form a preference for it over novel songs. When female zebra finches that were reared with their fathers were re-exposed to their fathers' song, they showed significantly greater neuronal activation in the caudomedial mesopallium (CMM), but not in the NCM or hippocampus, compared with when they were exposed to novel song. Neuronal activation in the NCM and CMM is not an artefact of isolation rearing, and is not related to attentional mechanisms. The NCM and the CMM might be parallel stores that contain the neural substrate for tutor (or father's) song memory, or the 'template'. The NCM might be more directly functionally linked to the premotor nuclei in the song system. The CMM overlaps with the intermediate and medial mesopallium (IMM) that contains the neural substrate for imprinting memory in domestic chicks. The NCM and CMM may be homologous with subdivisions of the mammalian auditory association cortex, which in humans are associated with auditory learning in relation to speech acquisition. Further multidisciplinary research is needed to determine whether the NCM and CMM contain the neural substrates of song memory, or whether this information is stored elsewhere in the brain. The neuroanatomical connectivity and functional relationship between these two brain regions and the song system needs to be investigated, in order for us to better understand the overall process of bird song learning. Such analyses may, ultimately, have heuristic value for the study of speech aquisition in humans. Birdsong learning in avian species has strong similarities with speech acquisition in human infants. Recent research on the song system has shed fresh light on the neural substrate of song memory and sensorimotor learning in both male and female songbirds. The process through which young male songbirds learn the characteristics of the songs of an adult male of their own species has strong similarities with speech acquisition in human infants. Both involve two phases: a period of auditory memorization followed by a period during which the individual develops its own vocalizations. The avian 'song system', a network of brain nuclei, is the probable neural substrate for the second phase of sensorimotor learning. By contrast, the neural representation of song memory acquired in the first phase is localized outside the song system, in different regions of the avian equivalent of the human auditory association cortex.

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: Animal communication / Animal Genetics and Genomics / Animals / Behavior, Animal / Behavioral psychophysiology / Behavioral Sciences / Biological and medical sciences / Biological Techniques / Biomedical and Life Sciences / Biomedicine / Birds / Brain - anatomy & histology / Brain - physiology / Brain research / Cognition & reasoning / Ear and associated structures. Auditory pathways and centers. Hearing. Vocal organ. Phonation. Sound production. Echolocation / Fundamental and applied biological sciences. Psychology / Learning / Male / Memory / Memory - physiology / Neural Pathways - anatomy & histology / Neural Pathways - physiology / Neurobiology / Neurosciences / Neurotransmission and behavior / Psychology. Psychoanalysis. Psychiatry / Psychology. Psychophysiology / review-article / Songbirds - anatomy & histology / Songbirds - blood / Songbirds - physiology / Testosterone - blood / Vertebrates: nervous system and sense organs / Vocalization, Animal - physiology