The present article responds to commentaries from experts in anthropology, apraxia, archeology, linguistics, neuroanatomy, neuroimaging, neurophysiology, neuropsychology, primatology, sign language emergence and sign language neurolinguistics on the book How the brain got language: The mirror system hypothesis (Arbib 2012). The role of complex imitation is discussed, and the distinction between protolanguage and language is emphasized. Issues debated include the role of protosign in scaffolding protospeech, the interplay between biological evolution of the brain and cultural evolution of the social interactions within groups, the relations brain mechanisms for action and language, and the question of when language first emerged.

The short answer to the question of How the Brain Got Language is “through biological and cultural evolution.” The challenge is to be more specific. I use the term “the language-ready brain” to suggest that the brain of early Homo sapiens was adequate to support language but that it required tens of millennia for humans to be able to exploit these innate neural capabilities to develop, cumulatively, languages and the societies that made languages possible and necessary. The ability to surf the World Wide Web is a recent example of society's expanding ability to develop technologies and social structures which allow humans to exploit their neural capabilities in ways that were not part of the adaptive pressures for biological evolution.

The two-fold challenge of the book, then, is to understand (i) what are the mechanisms of the language-ready brain and what adaptive pressures evolved them biologically; and (ii) how did those mechanisms support the emergence of language as well as modern-day patterns of language change, acquisition and use, and the social interactions which support them?

The article analyzes the neural and functional grounding of language skills as well as their emergence in hominid evolution, hypothesizing stages leading from abilities known to exist in monkeys and apes and presumed to exist in our hominid ancestors right through to modern spoken and signed languages. The starting point is the observation that both premotor area F5 in monkeys and Broca's area in humans contain a “mirror system” active for both execution and observation of manual actions, and that F5 and Broca's area are homologous brain regions. This grounded the mirror system hypothesis of Rizzolatti and Arbib (1998) which offers the mirror system for grasping as a key neural “missing link” between the abilities of our nonhuman ancestors of 20 million years ago and modern human language, with manual gestures rather than a system for vocal communication providing the initial seed for this evolutionary process. The present article, however, goes “beyond the mirror” to offer hypotheses on evolutionary changes within and outside the mirror systems which may have occurred to equip Homo sapiens with a language-ready brain. Crucial to the early stages of this progression is the mirror system for grasping and its extension to permit imitation. Imitation is seen as evolving via a so-called simple system such as that found in chimpanzees (which allows imitation of complex “object-oriented” sequences but only as the result of extensive practice) to a so-called complex system found in humans (which allows rapid imitation even of complex sequences, under appropriate conditions) which supports pantomime. This is hypothesized to have provided the substrate for the development of protosign, a combinatorially open repertoire of manual gestures, which then provides the scaffolding for the emergence of protospeech (which thus owes little to nonhuman vocalizations), with protosign and protospeech then developing in an expanding spiral. It is argued that these stages involve biological evolution of both brain and body. By contrast, it is argued that the progression from protosign and protospeech to languages with full-blown syntax and compositional semantics was a historical phenomenon in the development of Homo sapiens, involving few if any further biological changes.

In order to formulate hypotheses about the evolutionary underpinnings that preceded the first glimmerings of language, mother-infant gestural and vocal interactions are compared in chimpanzees and humans and used to model those of early hominins. These data, along with paleoanthropological evidence, suggest that prelinguistic vocal substrates for protolanguage that had prosodic features similar to contemporary motherese evolved as the trend for enlarging brains in late australopithecines/early Homo progressively increased the difficulty of parturition, thus causing a selective shift toward females that gave birth to relatively undeveloped neonates. It is hypothesized that hominin mothers adopted new foraging strategies that entailed maternal silencing, reassuring, and controlling of the behaviors of physically removed infants (i.e., that shared human babies' inability to cling to their mothers' bodies). As mothers increasingly used prosodic and gestural markings to encourage juveniles to behave and to follow, the meanings of certain utterances (words) became conventionalized. This hypothesis is based on the premises that hominin mothers that attended vigilantly to infants were strongly selected for, and that such mothers had genetically based potentials for consciously modifying vocalizations and gestures to control infants, both of which receive support from the literature.