Learning-induced neural plasticity of speech processing before birth

Learning-induced neural plasticity of speech processing before birth

1. Eino Partanen^a,^b,¹,
2. Teija Kujala^a,^c,
3. Risto Näätänen^a,^d,^e,
4. Auli Liitola^a,
5. Anke Sambeth^f, and
6. Minna Huotilainen^a,^b,^g

Author Affiliations

1. Edited by Michael I. Posner, University of Oregon, Eugene, OR, and approved July 22, 2013 (received for review February 1, 2013)

Significance

Learning, the foundation of adaptive and intelligent behavior, is based on changes in neural assemblies and reflected by the modulation of electric brain responses. In infancy, long-term memory traces are formed by auditory learning, improving discrimination skills, in particular those relevant for speech perception and understanding. Here we show direct neural evidence that neural memory traces are formed by auditory learning prior to birth. Our findings indicate that prenatal experiences have a remarkable influence on the brain’s auditory discrimination accuracy, which may support, for example, language acquisition during infancy. Consequently, our results also imply that it might be possible to support early auditory development and potentially compensate for difficulties of genetic nature, such as language impairment or dyslexia.

Abstract

Learning, the foundation of adaptive and intelligent behavior, is based on plastic changes in neural assemblies, reflected by the modulation of electric brain responses. In infancy, auditory learning implicates the formation and strengthening of neural long-term memory traces, improving discrimination skills, in particular those forming the prerequisites for speech perception and understanding. Although previous behavioral observations show that newborns react differentially to unfamiliar sounds vs. familiar sound material that they were exposed to as fetuses, the neural basis of fetal learning has not thus far been investigated. Here we demonstrate direct neural correlates of human fetal learning of speech-like auditory stimuli. We presented variants of words to fetuses; unlike infants with no exposure to these stimuli, the exposed fetuses showed enhanced brain activity (mismatch responses) in response to pitch changes for the trained variants after birth. Furthermore, a significant correlation existed between the amount of prenatal exposure and brain activity, with greater activity being associated with a higher amount of prenatal speech exposure. Moreover, the learning effect was generalized to other types of similar speech sounds not included in the training material. Consequently, our results indicate neural commitment specifically tuned to the speech features heard before birth and their memory representations.

• mismatch negativity
• event-related potentials

Footnotes

• ¹To whom correspondence should be addressed. E-mail: eino.partanen@helsinki.fi.

• Author contributions: E.P., T.K., A.L., and M.H. designed research; E.P. and A.L. performed research; E.P., A.L., and A.S. analyzed data; and E.P., T.K., R.N., and M.H. wrote the paper.
• The authors declare no conflict of interest.
• This article is a PNAS Direct Submission.
• This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1302159110/-/DCSupplemental.