Neurobiology of human language and its evolution: primate and non-primate perspectives
Constance Scharff, Angela D. Friederici, Michael Petrides
Specialty Chief Editor
Frontiers Media SA
Constance Scharff, Angela D. Friederici, Michael Petrides
Sarah E. Earp, Donna L. Maney
Since the time of Darwin, biologists have wondered whether birdsong and music may serve similar purposes or have the same evolutionary precursors. Most attempts to compare song with music have focused on the qualities of the sounds themselves, such as melody and rhythm. Song is a signal, however, and as such its meaning is tied inextricably to the response of the receiver. Imaging studies in humans have revealed that hearing music induces neural responses in the mesolimbic reward pathway. In this study, we tested whether the homologous pathway responds in songbirds exposed to conspecific song. We played male song to laboratory-housed white-throated sparrows, and immunolabeled the immediate early gene product Egr-1 in each region of the reward pathway that has a clear or putative homologue in humans. We found that the responses, and how well they mirrored those of humans listening to music, depended on sex and endocrine state. In females with breeding-typical plasma levels of estradiol, all of the regions of the mesolimbic reward pathway that respond to music in humans responded to song. In males, we saw responses in the amygdala but not the nucleus accumbens – similar to the pattern reported in humans listening to unpleasant music. The shared responses in the evolutionarily ancient mesolimbic reward system suggest that birdsong and music engage the same neuroaffective mechanisms in the intended listeners.
Donald F. Sacco, Karol Osipowicz
Christopher I. Petkov, Erich D. Jarvis
Vocal learners such as humans and songbirds can learn to produce elaborate patterns of structurally organized vocalizations, whereas many other vertebrates such as non-human primates and most other bird groups either cannot or do so to a very limited degree. To explain the similarities among humans and vocal-learning birds and the differences with other species, various theories have been proposed. One set of theories are motor theories, which underscore the role of the motor system as an evolutionary substrate for vocal production learning. For instance, the motor theory of speech and song perception proposes enhanced auditory perceptual learning of speech in humans and song in birds, which suggests a considerable level of neurobiological specialization. Another, a motor theory of vocal learning origin, proposes that the brain pathways that control the learning and production of song and speech were derived from adjacent motor brain pathways. Another set of theories are cognitive theories, which address the interface between cognition and the auditory-vocal domains to support language learning in humans. Here we critically review the behavioral and neurobiological evidence for parallels and differences between the so-called vocal learners and vocal non-learners in the context of motor and cognitive theories. In doing so, we note that behaviorally vocal-production learning abilities are more distributed than categorical, as are the auditory-learning abilities of animals. We propose testable hypotheses on the extent of the specializations and cross-species correspondences suggested by motor and cognitive theories. We believe that determining how spoken language evolved is likely to become clearer with concerted efforts in testing comparative data from many non-human animal species.
Taishi Kawamoto, Keiichi Onoda, Ken'ichiro Nakashima, Hiroshi Nittono, Shuhei Yamaguchi, Mitsuhiro Ura
People are typically quite sensitive about being accepted or excluded by others. Previous studies have suggested that the dorsal anterior cingulate cortex (dACC) is a key brain region involved in the detection of social exclusion. However, this region has also been shown to be sensitive to non-social expectancy violations. We often expect other people to follow an unwritten rule in which they include us as they would expect to be included, such that social exclusion likely involves some degree of expectancy violation. The present event-related functional magnetic resonance imaging (fMRI) study sought to separate the effects of expectancy violation from those of social exclusion, such that we employed an “overinclusion” condition in which a player was unexpectedly overincluded in the game by the other players. With this modification, we found that the dACC and right ventrolateral prefrontal cortex (rVLPFC) were activated by exclusion, relative to overinclusion. In addition, we identified a negative correlation between exclusion-evoked brain activity and self-rated social pain in the rVLPFC, but not in the dACC. These findings suggest that the rVLPFC is critical for regulating social pain, whereas the dACC plays an important role in the detection of exclusion. The neurobiological basis of social exclusion is different from that of mere expectancy violation.