Abstract
In the absence of clear phylogenetic data on the neurobiological basis of the evolution of language, comparative studies across species and across ontogenetic stages within humans may inform us about the possible neural prerequisites of language. In the adult human brain, language-relevant regions located in the frontal and temporal cortex are connected via different fiber tracts: ventral and dorsal pathways. Ontogenetically, it has been shown that newborns display an adult-like ventral pathway at birth. The dorsal pathway, however, seems to display two subparts which mature at different rates: one part, connecting the temporal cortex to the premotor cortex, is present at birth, whereas the other part, connecting the temporal cortex to Broca’s area, develops much later and is still not fully matured at the age of seven. At this age, typically developing children still have problems in processing syntactically complex sentences. We therefore suggest that the mastery of complex syntax, which is at the core of human language, crucially depends on the full maturation of the fiber connection between the temporal cortex and Broca’s area.
The neural basis of language evolution must remain speculative, since clear phylogenetic data are unavailable. However, there are two alternative, though more indirect ways, to approach this issue. One approach is to compare different species in their ability to learn language, in particular, syntax or rule-based sequences. A second is to consult ontogenetic data on language development and brain maturation, under the assumption that ontogeny to some extent reflects phylogeny. In this article, data from both approaches, with a strong focus on rule-based and syntactic sequence learning, will be discussed.
Central to the discussion is not only whether such sequences can be learned, but more crucially, what type of syntactic sequence can be learned. A fundamental distinction has been made between two grammar types, namely finite state grammars (FSG) following an (AB)n rule and phrase structure grammar (PSG) following an AnBn rule (Hauser et al., ; Fitch and Hauser, ; see Figure 1).
Figure 1
There are at least three possible mechanisms through which grammatical sequence learning can take place: (1) adjacent dependencies, as in (AB)n grammars, and also non-adjacent dependencies, which do not involve higher-order hierarchies, could be learned by extracting phonological regularities from the auditory input and memorizing these for further use; (2) adjacent dependencies between A and B in (AB)n grammars or between a determiner, e.g., the and a noun, e.g., man in natural grammars could be learned through the same mechanism described in (1), but without the buildup of a minimal hierarchy or (3) through the computation “Merge” that binds two elements into a minimal hierarchical structure (Chomsky,
In the following section, we will review the success of grammar learning in different species, discuss the possible underlying processing mechanisms, and debate their neural basis. The data from these studies examining this suggest that the three grammar learning mechanisms described above can be related to three different neural circuits: (1) an input-to-output circuit present in vocal learning animals, (2) a circuit subserving the learning of (AB)n structures, and (3) a circuit involving the learning of AnBn structures.
Grammar Learning Across Species
There are several studies that have taken a species-comparative approach. Some have compared artificial grammar learning between human and non-human primates, or have used similar grammar types to investigate songbirds’ ability to learn grammatical sequences. Others have additionally discussed the neural basis of these learning abilities.
Fitch and Hauser (
This difference in the structure of these pathways between humans and non-human primates is of particular interest in the light of a functional and structural imaging study in humans (Friederici et al.,
This conclusion, however, was challenged on both theoretical and empirical grounds. It has been argued that the processing of AnBn grammar does not necessarily require the buildup of a hierarchical structure, but could be based on a simpler computation involving a counting mechanism plus some memory abilities (Perruchet and Rey,
Figure 2

Artificial grammar used in Abe and Watanabe (
For humans, however, the argument can be made that the computation they apply to process symmetrical AnBn grammars does indeed involve hierarchy building. The argument is based on two findings. Humans process symmetrical grammatical structures lacking functional categories (Friederici et al.,
Figure 3

Structure and examples of German sentences used in Makuuchi et al. (
For songbirds, the argument concerning the mechanism underlying grammar learning is different. In songbirds, the ability to learn grammatical sequences is based on a brain system mediating auditory input-to-vocal output (Fujimoto et al.,
Language Development and Brain Maturation in Humans
In the past, the dorsal pathway that connects the temporal cortex to the frontal cortex, as observed in adults (Catani et al.,
Newborns and infants show impressive language learning abilities. Newborns learn simple grammatical rules from auditory input after brief exposure (Gervain et al.,
Figure 4

Fiber tracking of diffusion tensor imaging data with seed in Broca’s area and seed in the precentral gyrus/premotor cortex in (A) adults and (B) newborns. Two parts of the dorsal pathway are present in adults; one connecting the temporal cortex via the fasciculus arcuatus (AF) and the superior longitudinal fasciculus (SLF) to the inferior frontal gyrus, i.e., Broca’s area (blue), and one connecting the temporal cortex via the AF/SLF to the precentral gyrus, i.e., premotor cortex (yellow). In newborns, only the part connecting to the precentral gyrus can be detected. The ventral pathway connecting the ventral inferior frontal gyrus via the extreme capsule fiber to the temporal cortex (green) is detectable in adults and newborns. LH, left hemisphere.
Here, it is proposed that there are two functionally distinct parts of the dorsal pathway (see Figure 4): one part connecting the temporal cortex to the premotor cortex (hereafter called Dorsal Pathway I) and a second, more medially located part, connecting the temporal cortex to Broca’s area (hereafter called Dorsal Pathway II).
Dorsal Pathway I, supporting sensory-to-motor mapping, is present at birth, whereas Dorsal Pathway II is not (Perani et al.,
Dorsal Pathway II, connecting the temporal cortex to Broca’s area, only develops as the brain matures, and is not even fully myelinized at the age of seven (Brauer et al.,
Figure 5

Fiber tracking of diffusion tensor imaging data with seeds in Brodmann Area (BA) 44 and 45 in (A) adults and (B) 7-year-old children. The dorsal pathway connects the posterior part of Broca’s area (BA 44) to the temporal cortex via the AF/SLF. The ventral pathway connects the anterior part of Broca’s area (BA 45) to the temporal cortex via the extreme capsule fiber system.
These findings in humans make it likely that grammatical rule learning and processing in infants and in adults are partly based on different brain structures. Learning and processing of auditory structured sequences, as shown in infants, could be based on the ability to identify phonological statistical relations of elements in a sequence and some memory capacity. This ability may partly be based on Dorsal Pathway I. In adults, this automatic way of learning from the auditory input is no longer at work, and strategic processes take over (Mueller et al.,
Finally, the question remains: What is the function of the ventral pathway in language processing? The connection between the anterior portion of the prefrontal cortex and the middle temporal gyrus via the extreme capsule fiber system has been related functionally to semantic processing and comprehension (Saur et al.,
Conclusion
In light of these across species and within-human findings, we can speculate that there is a parallel mechanism for sequence learning across species, which is based on an auditory (input)-to-motor (output) circuit. In songbirds, the causal relation between the auditory input-to-vocal output and sequence learning is well established (Scharff and Nottebohm,
However, Dorsal Pathway II, connecting Broca’s area to the temporal cortex, may specifically subserve the processing of language-like hierarchical structures. The supporting evidence for this is twofold: first, the dorsal pathway is generally stronger in human adults than in non-human primates (Rilling et al.,
Statements
Acknowledgments
I thank the two reviewers and Jens Brauer for helpful comments on the manuscript.
Conflict of interest
The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
References
1
AbeK.WatanabeD. (2011). Songbirds possess the spontaneous ability to discriminate syntactic rules. Nat. Neurosci.14, 1067–1074.10.1038/nn.2869
2
AnwanderA.TittgemeyerM.von CramonD. Y.FriedericiA. D.KnöscheT. R. (2007). Connectivity-based parcellation of Broca’s area. Cereb. Cortex17, 816–825.10.1093/cercor/bhk034
3
BahlmannJ.SchubotzR.FriedericiA. D. (2008). Hierarchical artificial grammar processing engages Broca’s area. NeuroImage42, 525–534.10.1016/j.neuroimage.2008.04.249
4
BerwickR. C.OkanoyaK.BeckersG. J. L.BolhuisJ. J. (2011). Songs to syntax: the linguistics of birdsong. Trends Cogn. Sci. (Regul. Ed.)15, 113–121.10.1016/j.tics.2011.01.002
5
BloomfieldT. C.GentnerT. Q.MargoliashT. (2011). What birds have to say about language. Nat. Neurosci.14, 947–948.10.1038/nn.2884
6
BolhuisJ. J.OkanoyaK.ScharffC. (2010). Twitter evolution: converging mechanisms in birdsong and human speech. Nat. Rev. Neurosci.11, 747–759.10.1038/nrg2892
7
BornkesselI.ZyssettS.FriedericiA. D.von CramonD. Y.SchlesewskyM. (2005). Who did what to whom? The neural basis of argument hierarchies during language comprehension. Neuroimage26, 221–233.10.1016/j.neuroimage.2005.01.032
8
BrauerJ.AnwanderA.FriedericiA. D. (2011). Neuroanatomical prerequisites for language functions in the maturing brain. Cereb. Cortex21, 459–466.10.1093/cercor/bhq108
9
CataniM.HowardR. J.PajevicS.JonesD. K. (2002). Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage17, 77–94.10.1006/nimg.2002.1136
10
ChomskyN. (1995). The Minimalist Program. Cambridge, MA: MIT Press.
11
de Boysson-BardiesB.SagartL.DurantC. (1984). Discernible differences in the babbling of infants according to target language. J. Child Lang.11, 1–15.
12
de VriesM. H.MonaghanP.KnechtS.ZwitserloodP. (2008). Syntactic structure and artificial grammar learning: the learnability of embedded hierarchical structures. Cognition107, 763–774.10.1016/j.cognition.2007.09.002
13
Dehaene-LambertzG.Hertz-PannierL.DuboisJ.MériauxS.RocheA.SigmanM.DehaeneS. (2010). Functional organization of perisylvian activation during presentation of sentences in preverbal infants. Proc. Natl. Acad. Sci. U.S.A.103, 14240–14245.10.1073/pnas.0606302103
14
DittmarM.Abbot-SmithK.LievenE.TomaselloM. (2008). German children’s comprehension of word order and case marking in causative sentences. Child Dev.79, 1152–1167.10.1111/j.1467-8624.2008.01181.x
15
DuboisJ.Hertz-PannierL.CachiaA.ManginJ. F.Le BihanD.Dehaene-LambertzG. (2009). Structural asymmetries in the infant language and sensori-motor networks. Cereb. Cortex19, 414–423.10.1093/cercor/bhn097
16
DuboisJ.Hertz-PannierL.Dehaene-LambertzG.CointepasY.Le BihanaD. (2006). Assessment of the early organization and maturation of infants’ cerebral white matter fiber bundles: a feasibility study using quantitative diffusion tensor imaging and tractography. Neuroimage30, 1121–1132.10.1016/j.neuroimage.2005.11.022
17
FitchW. T.HauserM. D. (2004). Computational constraints on syntactic processing in a nonhuman primate. Science303, 377–380.10.1126/science.1089401
18
FriedericiA. D. (2009). Pathways to language: fiber tracts in the human brain. Trends Cogn. Sci. (Regul. Ed.)13, 175–181.10.1016/j.tics.2009.06.006
19
FriedericiA. D.BahlmannJ.HeimS.SchubotzR. I.AnwanderA. (2006). The brain differentiates human, and non-human grammars: functional localization, and structural connectivity. Proc. Natl. Acad. Sci. U.S.A.103, 2458–2463.10.1073/pnas.0509389103
20
FriedericiA. D.MakuuchiM.BahlmannJ. (2009). The role of the posterior superior temporal cortex in sentence comprehension. Neuroreport20, 563–568.10.1097/WNR.0b013e3283297dee
21
FriedericiA. D.MüllerJ.ObereckerR. (2011). Precursors to natural grammar learning: preliminary evidence from 4-month-old infants. PLoS ONE6, e17920.10.1371/journal.pone.0017920
22
FujimotoH.HasegawaT.WatanabeD. (2011). Neural coding of syntactic structure in learned vocalizations in the songbird. J. Neurosci.31, 10023–10033.10.1523/JNEUROSCI.1606-11.2011
23
GentnerT. Q.FennK. M.MargoliashD.NusbaumH. C. (2006). Recursive syntactic pattern learning by songbirds. Nature440, 1204–1207.10.1038/nature04675
24
GervainJ.MacagnoF.CogoiS.PenA. M.MehlerJ. (2008). The neonate brain detects speech structure. Proc. Natl. Acad. Sci. U.S.A.105, 14222–14227.10.1073/pnas.0806530105
25
GeschwindN. (1965a). Disconnexion syndromes in animals and man. I. Brain88, 237–294.10.1093/brain/88.2.237
26
GeschwindN. (1965b). Disconnexion syndromes in animals and man. II. Brain88, 585–644.10.1093/brain/88.2.237
27
HahneA.EcksteinK.FriedericiA. D. (2004). Brain signatures of syntactic and semantic processes during children’s language development. J. Cogn. Neurosci.16, 1302–1318.10.1162/0898929041920504
28
HauserM.ChomskyN.FitchW. (2002). The faculty of language: what is it, who has it, and how did it evolve?Science298, 1569–1579.10.1126/science.298.5598.1554d
29
HickokG.PoeppelD. (2007). The cortical organization of speech perception. Nat. Rev. Neurosci.8, 393–402.10.1038/nrn2113
30
KudoN.NonakaY.MizunoN.MizunoK.OkanoyaK. (2011) , On-line statistical segmentation of a non-speech auditory stream in neonates as demonstrated by event-related brain potentials. Dev. Sci.14, 1100–1106.10.1111/j.1467-7687.2011.01056.x
31
LeroyF.GlaselH.DuboisJ.Hertz-PannierL.ThirionB.ManginJ.-F.Dehaene-LambertzG. (2011). Early maturation of the linguistic dorsal pathway in human infants. J. Neurosci.31, 1500–1506.10.1523/JNEUROSCI.4141-10.2011
32
MakrisN.PandyaD. (2009). The extreme capsule in humans and rethinking of the language circuitry. Brain Struct. Funct.213, 343–358.10.1007/s00429-008-0199-8
33
MakuuchiM.BahlmannJ.AnwanderA.FriedericiA. D. (2009). Segregating the core computational faculty of human language from working memory. Proc. Natl. Acad. Sci. U.S.A.106, 8362–8367.10.1073/pnas.0810928106
34
MampeB.FriedericiA. D.ChristopheA.WermkeK. (2009). Newborns’ cry melody is shaped by their native language. Curr. Biol.19, 1994–1997.10.1016/j.cub.2009.09.064
35
MuellerJ. L.BahlmannJ.FriedericiA. D. (2010). Learnability of embedded syntactic structures depends on prosodic cues. Cogn. Sci.34, 338–349.10.1111/j.1551-6709.2009.01093.x
36
PeraniD.SaccumanM. C.ScifoP.AnwanderA.SpadaD.BaldoliC.PoloniatoA.LohmannG.FriedericiA. D. (2011). Neural language networks at birth. Proc. Natl. Acad. Sci. U.S.A.108, 16056–16061.10.1073/pnas.1102991108
37
PerruchetP.ReyA. (2005). Does the mastery of center-embedded linguistic structures distinguish humans from nonhuman primates?Psychon. Bull. Rev.12, 307–313.10.3758/BF03196377
38
PetridesM.PandyaD. (2009). Distinct parietal and temporal pathways to the homologues of Broca’s area in the monkey. PLoS Biol.7, e1000170.10.1371/journal.pbio.1000170
39
RillingJ. K.GlasserM. F.PreussT. M.MaX. Y.ZhaoT. J.HuX. P.BehrensT. E. J. (2008). The evolution of the arcuate fasciculus revealed with comparative DTI. Nat. Neurosci.11, 426–428.10.1038/nn2072
40
SaurD.KreherB. W.SchnellS.KümmererD.KellmeyerP.VryM. S.UmarovaR. M.GlaucheV.AbelS.HuberW.RijntjesM.HennigJ.WeillerC. (2008). Ventral and dorsal pathways for language. Proc. Natl. Acad. Sci. U.S.A.105, 18035–18040.10.1073/pnas.0805234105
41
ScharffC.NottebohmF. (1991). A comparative-study of the behavioral deficits following lesions of various parts of the zebra finch song system – implications for vocal learning. J. Neurosci.11, 2896–2913.
42
TeinonenT.FellmanV.NäätänenR.AlkuP.HuotilainenM. (2009). Statistical language learning in neonates revealed by event-related brain potentials. BMC Neurosci.10, 21.10.1186/1471-2202-10-21
43
TylerL. K.Marslen-WilsonW. D. (2008). Fronto-temporal brain systems supporting spoken language comprehension. Philos. Trans. R. Soc. Lond. B Biol. Sci.363, 1037–1054.10.1098/rstb.2007.2158
44
TylerL. K.Marslen-WilsonW. D.RandallB.WrightP.DevereuxB. J.ZhuangJ.PapoutsiM.StamatakisE. A. (2011). Left inferior frontal cortex and syntax: function, structure and behaviour in left-hemisphere damaged patients. Brain134, 415–431.10.1093/brain/awq369
45
WeillerC.BormannT.SaurD.MussoM.RijntjesM. (2011). How the ventral pathway got lost: and what its recovery might mean. Brain Lang.118, 29–39.10.1016/j.bandl.2011.01.005
46
WilsonS. M.GalantucciS.TartagliaM. C.RisingK.PattersonD. K.HenryM. L.OgarJ. M.DeLeonJ.MillerB. L.Gorno-TempiniM. L. (2011). Syntactic processing depends on dorsal language tracts. Neuron72, 397–403.10.1016/j.neuron.2011.09.014
Summary
Keywords
grammar, development, fiber tract, arcuate fasciculus
Citation
Friederici AD (2012) Language Development and the Ontogeny of the Dorsal Pathway. Front. Evol. Neurosci. 4:3. doi: 10.3389/fnevo.2012.00003
Received
06 October 2011
Accepted
18 January 2012
Published
06 February 2012
Volume
4 - 2012
Edited by
Constance Scharff, Freie Universitaet Berlin, Germany
Reviewed by
Steven Chance, Oxford University, UK; Paul M. Nealen, Indiana University of Pennsylvania, USA
Copyright
© 2012 Friederici.
This is an open-access article distributed under the terms of the Creative Commons Attribution Non Commercial License, which permits non-commercial use, distribution, and reproduction in other forums, provided the original authors and source are credited.
*Correspondence: Angela D. Friederici, Department of Neuropsychology, Max Planck Institute for Human Cognitive and Brain Sciences, Stephanstraße 1A, 04103 Leipzig, Germany. e-mail: angelafr@cbs.mpg.de
Disclaimer
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.