Learning-induced neural plasticity of speech processing before birth

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 D uring the fetal period the brain undergoes extensive developmental changes as new synapses are formed (1) and axonal connections between neurons are myelinated (2), facilitating efficient recognition and analysis of complex information. In audition, the functional maturation of the developing nervous system is driven by external input, which is evidenced by, for instance, the rapid reorganization of the auditory cortex by external stimuli soon after the onset of hearing in rats (3). This was suggested to occur in humans usually by the gestational age of 27 wk (4). Such plastic changes in neural assemblies during early development indicate that humans have some learning capability even before birth (5, 6). However, this learning capability may be based predominantly on the discrimination of low-pitched sounds that can penetrate the intrauterine walls (7-9). This lowpitch information may play an important role in early speech discrimination of newborns (10) by facilitating learning to segment incoming speech into meaningful units.Consistent with this, previous behavioral studies have shown that fetuses become attuned to a variety of features of the surrounding auditory environment. For example, fetuses habituate to the native language of the environment or of the mother (11, 12), familiar melodies (13) or fragments of stories heard during pregnancy (14), and even the mother's voice (15). In addition to learning-based habituation involving the laterobasal amygdala only (16), fetuses, for example, react differently to native and nonnative vowels (17) or f...

The Sooner, the Better

“…Research shows that children are sensitive to language even prenatally (Moon et al, 2013;Partanen et al, 2013), yet in the first few months after a child is born, general language experiences are more likely to make a difference than reading aloud. However, as no negative effects of a very early start of reading to a child are to be expected, the sooner the better appears to be best.…”

“…Children's language and literacy competence does not begin when children enter school-Children's literacy learning starts well before formal schooling, and studies have shown that children are sensitive to speech even prenatally (e.g., Moon, Lagercrantz, & Kuhl, 2013;Partanen et al, 2013). Parents and primary caregivers (subsequently referred to as parents) are highly influential in a child's early learning as parent-child interactions are frequent and ongoing.…”

Mother’s voice and heartbeat sounds elicit auditory plasticity in the human brain before full gestation

“…Similarly, Beauchemin et al have found activation in language-related cortical regions when newborns listened to their mother's voice, whereas a stranger's voice seemed to activate more generic regions of the brain (20). In addition, Partanen et al have shown that the neural response to maternal sounds depends on experience as full-term newborns react differentially to familiar vs. unfamiliar sounds they were exposed to as fetuses, suggesting correlation between the amount of prenatal exposure and brain activity (21). Taken together, the above studies suggest that the mother's voice plays a special role in the early shaping of auditory and language areas of the brain.…”

Brain regions and functional interactions supporting early word recognition in the face of input variability

“…Developmental studies in the language domain have uncovered basic perceptual (4-6), discrimination (7,8), and mnemonic capacities (9)(10)(11)(12)(13)(14) in newborns and fetuses, supporting the hypothesis that memories for sounds begin to be established very early in life. However, infants' memory for specific words seems to be highly vulnerable to interference.…”