Communicative ontogeny

The ontogeny of communication stems from a latent genetic potential. This is channelled, constrained, and developed through the neonatal environment (Aitken Reference Aitken2008; Aitken & Trevarthen Reference Aitken and Trevarthen1997; Crais et al. Reference Crais, Douglas and Campbell2004; Rowe & Goldin-Meadow Reference Rowe and Goldin-Meadow2009). Neonates interact with adults with varied communicative capabilities. Over 100,000 years, newborns have adapted to massive changes in culture and language, while the genetic mechanisms proposed are largely unchanged

Prehistoric behaviour left us no records. We have to look to contemporary ontogenies to observe differences in development. Signing-for-communication by the congenitally deaf infants of signing deaf parents is precocious, while infants with hearing parents and hearing infants with congenitally deaf parents are often slow in signing (Volterra & Erting Reference Volterra and Erting1990). Language and social attunement in hearing infants with hearing parents seems little affected by variations in adult gesture (Kirk et al. Reference Kirk, Howlett, Pine and Fletcher2012). Interactional attunement seems critical to infant development (Lundy Reference Lundy2013).

Ontogeny only partially mirrors phylogeny. The communicative environment guides our latent and flexible potential. Our neonatal capacity to cope with, adapt to, and rapidly learn from our social environment is perhaps the unique human attribute. We are born with the capacity to develop the language of our parents through their environment. We are socially altricial – our larger cortices enable us to immerse ourselves in and learn through our social environment, to engage our caregivers and to ensure that we are cared for and stimulated. This process is largely articulated well before we develop language (Feldman Reference Feldman2007; Oller et al. Reference Oller, Buder, Ramsdell, Chorna, Warlaumont and Bakeman2013).

Foetal brain growth approaches the limits imposed by maternal pelvic size. This is at the cost of the neotenous development and relative vulnerability of most other organ systems. Accelerated early postnatal growth could surely achieve this end to support a cognitive-linguistic system with reduced perinatal risk. The abilities necessary to social survival relies on the intergenerational transmission of adaptability. A dyadic preverbal system underpins this process (see Trevarthen & Aitken Reference Trevarthen and Aitken2001), but the “second-person neuroscience” required to study its neurobiology is a recent development (Schilbach et al. Reference Schilbach, Timmermans, Reddy, Costall, Bente, Schlicht and Vogeley2013).

An alternative evolutionary strategy, typified by the social insects, relies on invariance in the social behaviour of its members (see Miller Reference Miller2010). This can also provide evolutionary success but is less robust in the face of significant environmental change.

FOXP2 – “Human-specific and central to linguistic communication” or a more general key in processing complex information?

Forkhead transcription factors are important to a wide range of developmental processes (Carlsson & Mahlapuu Reference Carlsson and Mahlapuu2002; Nudel & Newbury Reference Nudel and Newbury2013). Interest in FOXP2 came through studying the effects of its mutation on one family pedigree – the KE family (Lai et al. Reference Lai, Fisher, Hurst, Vargha-Khadem and Monaco2001). First referred to as a “developmental verbal dyspraxia” (Hurst et al. Reference Hurst, Baraitser, Auger, Graham and Norell1990), it has also been reported simply as a “dysphasia” (Gopnik Reference Gopnik1990b), as a defect in phonology and language-production (Fletcher Reference Fletcher1990), and a severe speech disorder affecting all aspects of expressive language (Vargha-Khadem & Passingham Reference Vargha-Khadem and Passingham1990). Non-language–related differences have also been reported (Liégeois et al. Reference Liégeois, Baldeweg, Connelly, Gadian, Mishkin and Vargha-Khadem2003).

FOXP2 is highly conserved. Only two amino acids differentiate us from orthologs in certain other primates (such as the gorilla and chimpanzee), and three from the orang-utan and mouse. In mice, a defect in FoxP2 impairs both ultrasonic vocalization (Shu et al. Reference Shu, Cho, Jiang, Zhang, Weisz, Elder, Schmeidler, De Gasperi, Gama Sosa, Rabidou, Santucci, Perl, Morrisey and Buxbaum2005) and motor learning (Groszer et al. Reference Groszer, Keays, Deacon, de Bono, Prasad-Mulcare, Gaub, Baum, French, Nicod, Coventry, Enard, Fray, Brown, Nolan, Pääbo, Channon, Costa, Ellers, Ehret, Rawlins and Fisher2008), and there are sex differences in gene expression (Bowers et al. Reference Bowers, Perez-Pouchoulen, Edwards and McCarthy2013). In the human, FOXP transcription differences, including FOXP2, are associated with an increased likelihood of autism spectrum disorders (ASD) (see Bowers & Konopka Reference Bowers and Konopka2012; Mukamel et al. Reference Mukamel, Konopka, Wexler, Osborn, Dong, Bergman, Levitt and Geschwind2011; Toma et al. Reference Toma, Hervásk, Torrico, Balmañnak, Salgado, Maristany, Vilella, Martínez-Leal, Planelles, Cuscóc, del Campo, Pérez-Jurado, Caballero-Andaluz, de Diego-Otero, Pérez-Costillas, Ramos-Quiroga, Ribasés, Bayés and Cormand2013).

Is FOXP2 the key “language gene”?

A group of genetic factors is reported in association with specific language impairments (SLIs). These include FOXP2, CYP19A1, FOXG1, FOXP1, NRXN1, PCDH11X, PCDH11Y, SETBP1, CNTNAP2, ATP2C2, and CMIP (Deriziotis & Fisher Reference Deriziotis and Fisher2013; Marseglia et al. Reference Marseglia, Scordo, Pescucci, Nannetti, Biagini, Scandurra, Gerundino, Magi, Benelli and Torricelli2012; Newbury et al. Reference Newbury, Fisher and Monaco2010; Toma et al. Reference Toma, Hervásk, Torrico, Balmañnak, Salgado, Maristany, Vilella, Martínez-Leal, Planelles, Cuscóc, del Campo, Pérez-Jurado, Caballero-Andaluz, de Diego-Otero, Pérez-Costillas, Ramos-Quiroga, Ribasés, Bayés and Cormand2013). SLIs are commonly reported in association with ASD (Bowers & Konopka Reference Bowers and Konopka2012; Chien et al. Reference Chien, Gau, Chen, Tsai, Wu, Chen, Shang and Chen2013; Szalontai & Csiszar Reference Szalontai and Csiszar2013). In addition, CNTNAP2 KIIA0319/TTRAP/THEM2 mutations have been reported in association with reading disorders (see Newbury et al. Reference Newbury, Paracchini, Scerri, Winchester, Addis, Richardson, Walter, Stein, Talcott and Monaco2011; Pinel et al. Reference Pinel, Fauchereau, Moreno, Barbot, Lathrop, Zelenika, Le Bihan, Poline, Bourgeron and Dehaene2012).

Is the specialised role of FOXP2 confined to human communication?

Orthologs of the FOXP2 gene are found across many species, affect vocal communication in many. It is highly conserved and seems likely to have an important function or functions preceding its role in language. The notion of “deep homology” of structural genes in somatotopic development is well known, but its relevance to social behaviour has only recently been suggested (Scharff & Petri Reference Scharff and Petri2011). Overly strong parallels to animal models are inappropriate (see Lynch Reference Lynch2009), however knock-in “humanized” FoxP2 genes in mice have been shown to alter cortico-basal ganglia circuitry (Enard et al. Reference Enard, Gehre, Hammerschmidt, Hölter, Blass, Somel, Brückner, Schreiweis, Winter, Sohr, Becker, Wiebe, Nickel, Giger, Müller, Groszer, Adler, Aguilar, Bolle, Calzada-Wack, Dalke, Ehrhardt, Favor, Fuchs, Gailus-Durner, Hans, Hölzlwimmer, Javaheri, Kalaydjiev, Kallnik, Kling, Kunder, Mossbrugger, Naton, Racz, Rathkolb, Rozman, Schrewe, Busch, Graw, Ivandic, Klingenspor, Klopstock, Ollert, Quintanilla-Martinez, Schulz, Wolf, Wurst, Zimmer, Fisher, Morgenstern, Arendt, de Angelis, Fischer, Schwarz and Pääbo2009).

FoxP2 is involved in complex non-linguistic systems. It affects birdsong development (Teramitsu et al. Reference Teramitsu, Kudo, London, Geschwind and White2004), and FoxP2 protein levels alter with the amount of male singing (Miller et al. Reference Miller, Spiteri, Condro, Dosumu-Johnson, Geschwind and White2008). In some species of bat, FoxP2 appears to have evolved in parallel with echolocation (Yin et al. Reference Yin, Ma, Zhang and Metzner2008). Here, complex vocalization is used to coordinate flight and prey location (see Metzner & Schuller Reference Metzner, Schuller and Brudzynski2010).

FoxP2 has undergone accelerated evolution in echolocating bats (Li et al. Reference Li, Wang, Rossiter, Jones and Zhang2007), whales, dolphins (Nery et al. Reference Nery, González and Opazo2013), and humans (Ayub et al. Reference Ayub, Yngvadottir, Chen, Xue, Hu, Vernes, Fisher and Tyler-Smith2013). It has a wider range of functions, across a broader phylogenetic range than was previously appreciated in the brain networks for complex auditory processing. In some species this has served communication, while in others its adaptive function seems more related to complex motor guidance.

Targets in the avian and human brain are now clearer, but their genetic effects and neurochemical cascade are complex (Konopka et al. Reference Konopka, Bomar, Winden, Coppola, Jonsson, Gao, Peng, Preuss, Wohlschlegel and Geschwind2009). To date, some 34 FOXP2 transcription targets have been identified in basal ganglia and inferior frontal cortex alone (Spiteri et al. Reference Spiteri, Konopka, Coppola, Bomar, Oldham, Ou, Vernes, Fisher, Ren and Geschwind2007).

FOXP2 is insufficient to account for the development of human language or its neural and neurochemical substrates. It is a proxy marker for the genetic control of complex biological systems we are only beginning to define or understand.