It has long been suggested that early language learning experience impacts later development1, but what is not known is how this is related to underlying neural organization. Here we show, strikingly, that even relatively short delays in exposure to French, and/or early exposure to another language, lead to different neural patterns for processing the sounds of that language than is found in native speakers. Although our three learner groups were all highly proficient speakers of French and had had many years of experience with that language, the differences in language learning that they experienced within their first 3 years of life appear to have affected their patterns of brain activation years later as assessed by a PWM task in French. Crucially, this occurred even in cases where the birth language had been discontinued and participants had become monolingual speakers of their second language, French, underscoring the unique contribution of early experiences on neural processing of a later learned language.

It would appear, in our participants, that early exposure to Chinese and/or delayed exposure to French affected the brain activation patterns that are typically involved in working memory processing, including brain areas that are more strongly activated by verbal stimuli or language sounds17, as well as regions more typically associated with non-verbal working memory and those involved in more general attention and cognitive control14,23. In relation to the former, highly proficient French-speaking IA children and Chinese–French bilinguals, who experienced very short delays in exposure to French, recruited left inferior frontal gyrus and anterior insula more weakly when processing French phonological units in unfamiliar French-like stimuli than monolingual French speakers. While the insular region has been implicated as a key area in a variety of general cognitive functions and is a hub in proposed salience, central executive and default mode networks32,33, the left anterior insula has also been found to be active during verbal or PWM processing in a way that differs from these more general mechanisms. For example, in response to verbal memory tasks the left, in contrast to the right, anterior insula is more strongly activated14,15, and this typically occurs along with several ‘classic’ frontal, temporal and parietal language regions with which the left insula shares functional and structural connections21,22. That the French monolinguals in the present study showed greater activation than the other groups in the left anterior insula, that this activation extended into inferior frontal gyrus in the left hemisphere only, and that functional connectivity was observed between left insula and other left-lateralized regions typically implicated in the PWM network, together suggest more ‘language-specific’ processing of these French sounds by this group who was exposed to French from birth. Concomitantly, weaker recruitment of this region in the IA and bilingual participants may reflect the processing of these French sounds within a neural system that was initially set-up to process a different language. Of note, such findings do not mean that left insula cannot be recruited when processing non-native phonology. Indeed, other studies have reported such activation23,34,35,36, and all groups in the present study demonstrated left insular activation to some degree. However, the present results indicate that the insula may not be recruited in the same way or to the same extent as it is during native language processing.

In contrast to the typical PWM activation pattern observed in the French monolingual participants, the bilingual and IA participants more strongly activated several areas that have been implicated in non-verbal memory tasks14, as well as attentional, goal directed and cognitive control processes23,26,27. Indeed, both the bilingual and IA participants, but not the French monolinguals, strongly recruited right middle frontal gyrus/posterior superior frontal gyrus (BA 6) and left medial frontal cortex in regions that precisely matched those observed in a meta-analysis that implicated these regions in non-verbal, as opposed to verbal, memory processing14. In contrast, the monolingual speakers activated bilateral middle/superior frontal gyrus (BA 9), which is commonly implicated in verbal memory processing21. Moreover, the bilingual and IA participants both activated bilateral superior temporal gyrus (STG; right >left) more strongly than the French monolinguals. Prior research has demonstrated greater bilateral activation during language tasks37, particularly in frontal, temporal and parietal regions38 for bilinguals who acquired their second language early in life, consistent with the experience of our bilingual group. Furthermore, right hemisphere STG activation has typically been associated with the processing of music and non-language sounds, in contrast to fine-grained phonetic discriminations of the kind required in the present study39,40.

Greater bilateral activation of several brain regions, as well as additional recruitment of attention and cognitive control regions, has previously been shown in bilingual speakers who are thought to use executive and cognitive control functions during the online use of two languages26. However, it is noteworthy in the present study that a similar pattern was also observed in the IA participants whose only exposure to another language had been discontinued years earlier. The activation of these regions by both the IA and bilingual groups, who performed this PWM task with high speed and accuracy, suggests that they drew on alternative systems to attain the same level of performance as the monolinguals. This interpretation is supported by previous studies in which structural changes in frontal, temporal and parietal regions involved in cognitive control41, as well as greater connectedness and efficiency in subnetworks involved in language monitoring42, have been observed in bilinguals in comparison to monolinguals, particularly as proficiency increases41. In the present study, more exposure to French was associated with greater activation in frontal and temporal/parietal brain areas that are comparable to those shown in these studies, suggesting that engagement of these executive and cognitive control regions may allow for increasingly efficient and proficient processing of a second language overtime43. This speaks to the remarkable flexibility of the brain to adapt to changing environmental circumstances and to engage alternative neural systems in new learning if other systems are not as readily available or relevant. Moreover, the similarities observed between IA and bilingual participants’ brain activation patterns imply that even relatively early language experiences influence the way this system is established and subsequently used. These similarities may also suggest a relationship between early language experience and the development of executive function, particularly as it relates to cognitive advantages that have been observed in bilinguals28. This would be an interesting area for future research. Given that our participants were children and adolescents (ranging in age from 10 to 17 years at the time of testing), we were not able to determine whether or how this impacted their earlier development, when they were first acquiring French, nor whether these effects extend past adolescence into adulthood.

We assume that the neural processing differences observed between the present groups were due to the early establishment of neural representations for a language other than French (that is, Chinese). Evidence that early-established neural representations are, in fact, maintained over time comes not only from the present study, but also from a prior investigation of the same IA participants that examined the neural maintenance of their discontinued first language—Chinese5. Results from that study showed that the IA participants, who had early but discontinued exposure to Chinese, recruited the same brain regions when processing Chinese lexical tone as Chinese–French bilingual speakers who had spoken Chinese since birth. Crucially, even though the IA participants had been exposed to and used French exclusively since adoption, they showed activation that differed from the French monolinguals. Together with the current findings, this provides strong evidence that neural representations acquired during the earliest stages of development are maintained across time even in the absence of continued exposure to the source of that information. The former results5 demonstrate the maintenance of neural templates even when a language is discontinued, while the present study extends this finding to suggest that these templates have an ongoing and lasting impact on the processing of subsequently learned language sounds. While we have examined a tonal/non-tonal language pairing, it would also be interesting to assess the effect of early language experience on subsequent neural outcomes in other language pairs, perhaps as a function of language similarity. Indeed, there is some evidence that L2 processing might be more likely to recruit distinct brain areas if the L2 is dissimilar to the L1 (for example, Chinese versus English44). Thus, it would be interesting to examine processing of an L2 that is relatively similar to the L1 of participants, such as Spanish and French, in contrast to the language pairs examined in the present study that are very different, to see if the same pattern of results is obtained.

Principles supporting our interpretation have been shown in other species. For example, rats that have previously learned a spatial navigation task45 or a fear-conditioning task46 acquire a second version of the task via fundamentally distinct molecular mechanisms. This is because memory traces underlying the first task require that the animals learn the second task in a different way, by building on these earlier traces. Rather than recruiting the mechanisms necessary for first-time learning, new mechanisms were recruited to update previously established traces with new representations. Similarly, our work suggests that if infants acquire a system of phonological representations for one language, the phonology of a second language may subsequently be acquired or processed via distinct mechanisms that build on this early system. If this is the case, then the neural processing of French pseudo-words by the IA and bilingual participants in the present study might thus be argued to reflect the processing of new information within a system based on previously acquired neural representations that have been maintained overtime. Note that this does not imply that second-language learners will not recruit the same brain regions as native speakers when processing any aspect of their second language. Indeed, it has been demonstrated that certain neural patterns come to resemble those of native speakers as second-language learners’ proficiency increases47. However, the results from the present study suggest that proficiency may not be the whole story; thus, beginning to elucidate the dynamic interaction between proficiency, the timing of language experience, and the neural representations of language and language sounds48.

In summary, the present study provides neural evidence that very early language experiences have a lasting influence on the way the brain processes the sounds of a language. We suggest that this is due to representations established from input in the first language that have persisted over time to influence the processing of second-language phonology. The fact that these neural differences did not preclude the achievement of equally advanced language proficiency highlights the incredibly adaptable ways that the brain is able to respond to a variety of language-learning circumstances.