Effects of early adversity on neural mechanisms of distractor suppression are mediated by sympathetic nervous system activity in preschool-aged children.

Multiple theoretical frameworks posit that interactions between the autonomic nervous system and higher-order neural networks are crucial for cognitive regulation. However, few studies have simultaneously examined autonomic physiology and brain activity during cognitive tasks. Such research is promising for understanding how early adversity impacts neurocognitive development in children, given that stress experienced early in life impacts both autonomic function and regulatory behaviors. We recorded event-related potentials (ERPs) as a neural measure of auditory selective attention, and cardiovascular measures of high-frequency heart rate variability (HF-HRV) and preejection period (PEP), in 105 3-5-year-old children with varying degrees of socioeconomic risk. First, we replicated a previous study from our lab: Increased socioeconomic risk was associated with larger ERP amplitudes elicited by distracting sounds. Next, we tested whether PEP and HF-HRV (at rest and during the task) were associated with the distractor ERP response, and found that a physiological profile marked by heightened sympathetic nervous system activity, indexed by shorter PEP, was associated with better ERP suppression of distractor sounds in lower SES children. Finally, we found that PEP mediated the relationship between socioeconomic risk and larger ERP responses to distractor sounds. In line with similar reports, these results suggest that for lower SES children, there is a potential biological cost of achieving better cognitive performance, seen here as increased cardiovascular arousal both at rest and in response to task demands. (PsycINFO Database Record

Parasympathetic and sympathetic activity are associated with individual differences in neural indices of selective attention in adults.

Multiple theoretical frameworks posit that interactions between the autonomic nervous system and higher-order neural networks are crucial for cognitive and emotion regulation. However, few studies have directly examined the relationship between measures of autonomic physiology and brain activity during cognitive tasks, and fewer studies have examined both the parasympathetic and sympathetic autonomic branches when doing so. Here, 93 adults completed an ERP auditory selective attention task concurrently with measures of parasympathetic activity (high-frequency heart rate variability; HF-HRV) and sympathetic activity (preejection period; PEP). We focus on the well-studied N1 ERP component to test for associations with baseline values of HF-HRV and PEP. Individuals with higher resting HF-HRV and shorter resting PEP showed larger effects of selective attention on their ERPs. Follow-up regression models demonstrated that HF-HRV and PEP accounted for unique variance in selective attention effects on N1 mean amplitude. These results are consistent with the neurovisceral integration model, such that greater parasympathetic activity is a marker of increased selective attention, as well as other theoretical models that emphasize the role of heightened sympathetic activity in more efficient attention-related processing. The present findings highlight the importance of autonomic physiology in the study of individual differences in neurocognitive function and, given the foundational role of selective attention across cognitive domains, suggest that both parasympathetic and sympathetic activity may be key to understanding variability in brain function across a variety of cognitive tasks.

Anterior and posterior erp rhyming effects in 3- to 5-year-old children.

During early literacy skills development, rhyming is an important indicator of the phonological precursors required for reading. To determine if neural signatures of rhyming are apparent in early childhood, we recorded event-related potentials (ERPs) from 3- to 5-year-old, preliterate children (N = 62) in an auditory prime-target nonword rhyming paradigm (e.g., bly-gry, blane-vox). Overall, nonrhyming targets elicited a larger negativity (N450) than rhyming targets over posterior regions. In contrast, rhyming targets elicited a larger negativity than nonrhyming targets over fronto-lateral sites. The amplitude of the two rhyming effects was correlated, such that a larger posterior effect occurred with a smaller anterior effect. To determine whether these neural signatures of rhyming related to phonological awareness, we divided the children into two groups based on phonological awareness scores while controlling for age and socioeconomic status. The posterior rhyming effect was stronger and more widely distributed in the group with better phonological awareness, whereas differences between groups for the anterior effect were small and not significant. This pattern of results suggests that the rhyme processes indexed by the anterior effect are developmental precursors to those indexed by the posterior effect. Overall, these findings demonstrate early establishment of distributed neurocognitive networks for rhyme processing.

Neuroplasticity of selective attention: Research foundations and preliminary evidence for a gene by intervention interaction.

This article reviews the trajectory of our research program on selective attention, which has moved from basic research on the neural processes underlying selective attention to translational studies using selective attention as a neurobiological target for evidence-based interventions. We use this background to present a promising preliminary investigation of how genetic and experiential factors interact during development (i.e., gene × intervention interactions). Our findings provide evidence on how exposure to a family-based training can modify the associations between genotype (5-HTTLPR) and the neural mechanisms of selective attention in preschool children from lower socioeconomic status backgrounds.

Atypical white-matter microstructure in congenitally deaf adults: A region of interest and tractography study using diffusion-tensor imaging.

Considerable research documents the cross-modal reorganization of auditory cortices as a consequence of congenital deafness, with remapped functions that include visual and somatosensory processing of both linguistic and nonlinguistic information. Structural changes accompany this cross-modal neuroplasticity, but precisely which specific structural changes accompany congenital and early deafness and whether there are group differences in hemispheric asymmetries remain to be established. Here, we used diffusion tensor imaging (DTI) to examine microstructural white matter changes accompanying cross-modal reorganization in 23 deaf adults who were genetically, profoundly, and congenitally deaf, having learned sign language from infancy with 26 hearing controls who participated in our previous fMRI studies of cross-modal neuroplasticity. In contrast to prior literature using a whole-brain approach, we introduce a semiautomatic method for demarcating auditory regions in which regions of interest (ROIs) are defined on the normalized white matter skeleton for all participants, projected into each participants native space, and manually constrained to anatomical boundaries. White-matter ROIs were left and right Heschl's gyrus (HG), left and right anterior superior temporal gyrus (aSTG), left and right posterior superior temporal gyrus (pSTG), as well as one tractography-defined region in the splenium of the corpus callosum connecting homologous left and right superior temporal regions (pCC). Within these regions, we measured fractional anisotropy (FA), radial diffusivity (RD), axial diffusivity (AD), and white-matter volume. Congenitally deaf adults had reduced FA and volume in white matter structures underlying bilateral HG, aSTG, pSTG, and reduced FA in pCC. In HG and pCC, this reduction in FA corresponded with increased RD, but differences in aSTG and pSTG could not be localized to alterations in RD or AD. Direct statistical tests of hemispheric asymmetries in these differences indicated the most prominent effects in pSTG, where the largest differences between groups occurred in the right hemisphere. Other regions did not show significant hemispheric asymmetries in group differences. Taken together, these results indicate that atypical white matter microstructure and reduced volume underlies regions of superior temporal primary and association auditory cortex and introduce a robust method for quantifying volumetric and white matter microstructural differences that can be applied to future studies of special populations.

5-HTTLPR polymorphism is linked to neural mechanisms of selective attention in preschoolers from lower socioeconomic status backgrounds.

While a growing body of research has identified experiential factors associated with differences in selective attention, relatively little is known about the contribution of genetic factors to the skill of sustained selective attention, especially in early childhood. Here, we assessed the association between the serotonin transporter linked polymorphic region (5-HTTLPR) genotypes and the neural mechanisms of selective attention in young children from lower socioeconomic status (SES) backgrounds. Event-related potentials (ERPs) were recorded during a dichotic listening task from 121 children (76 females, aged 40-67 months), who were also genotyped for the short and long allele of 5-HTTLPR. The effect of selective attention was measured as the difference in ERP mean amplitudes elicited by identical probe stimuli embedded in stories when they were attended versus unattended. Compared to children homozygous for the long allele, children who carried at least one copy of the short allele showed larger effects of selective attention on neural processing. These findings link the short allele of the 5-HTTLPR to enhanced neural mechanisms of selective attention and lay the groundwork for future studies of gene-by-environment interactions in the context of key cognitive skills.

Individual differences in neural mechanisms of selective auditory attention in preschoolers from lower socioeconomic status backgrounds: an event-related potentials study.

Selective attention, the ability to enhance the processing of particular input while suppressing the information from other concurrent sources, has been postulated to be a foundational skill for learning and academic achievement. The neural mechanisms of this foundational ability are both vulnerable and enhanceable in children from lower socioeconomic status (SES) families. In the current study, we assessed individual differences in neural mechanisms of this malleable brain function in children from lower SES families. Specifically, we investigated the extent to which individual differences in neural mechanisms of selective auditory attention accounted for variability in nonverbal cognitive abilities in lower SES preschoolers. We recorded event-related potentials (ERPs) during a dichotic listening task and administered nonverbal IQ tasks to 124 lower SES children (77 females) between the ages of 40 and 67 months. The attention effect, i.e., the difference in ERP mean amplitudes elicited by identical probes embedded in stories when attended versus unattended, was significantly correlated with nonverbal IQ scores. Larger, more positive attention effects over the anterior and central electrode locations were associated with superior nonverbal IQ performance. Our findings provide initial evidence for prominent individual differences in neural indices of selective attention in lower SES children. Furthermore, our results indicate a noteworthy relationship between neural mechanisms of selective attention and nonverbal IQ performance in lower SES preschoolers. These findings provide the basis for future research to identify the factors that contribute to such individual differences in neural mechanisms of selective attention.

Visual working memory continues to develop through adolescence.

The capacity of visual working memory (VWM) refers to the amount of visual information that can be maintained in mind at once, readily accessible for ongoing tasks. In healthy young adults, the capacity limit of VWM corresponds to about three simple objects. While some researchers argued that VWM capacity becomes adult-like in early years of life, others claimed that the capacity of VWM continues to develop beyond middle childhood. Here we assessed whether VWM capacity reaches adult levels in adolescence. Using an adaptation of the visual change detection task, we measured VWM capacity estimates in 13-year-olds, 16-year-olds, and young adults. We tested whether the capacity estimates observed in early or later years of adolescence were comparable to the estimates obtained from adults. Our results demonstrated that the capacity of VWM continues to develop throughout adolescence, not reaching adult levels even in 16-year-olds. These findings suggest that VWM capacity displays a prolonged development, similar to the protracted trajectories observed in various other aspects of cognition.

Implicit and explicit contributions to statistical learning.

Statistical learning allows learners to detect regularities in the environment and appears to emerge automatically as a consequence of experience. Statistical learning paradigms bear many similarities to those of artificial grammar learning and other types of implicit learning. However, whether learning effects in statistical learning tasks are driven by implicit knowledge has not been thoroughly examined. The present study addressed this gap by examining the role of implicit and explicit knowledge within the context of a typical auditory statistical learning paradigm. Learners were exposed to a continuous stream of repeating nonsense words. Learning was tested (a) directly via a forced-choice recognition test combined with a remember/know procedure and (b) indirectly through a novel reaction time (RT) test. Behavior and brain potentials revealed statistical learning effects with both tests. On the recognition test, accurate responses were associated with subjective feelings of stronger recollection, and learned nonsense words relative to nonword foils elicited an enhanced late positive potential indicative of explicit knowledge. On the RT test, both RTs and P300 amplitudes differed as a function of syllable position, reflecting facilitation attributable to statistical learning. Explicit stimulus recognition did not correlate with RT or P300 effects on the RT test. These results provide evidence that explicit knowledge is accrued during statistical learning, while bringing out the possibility that dissociable implicit representations are acquired in parallel. The commonly used recognition measure primarily reflects explicit knowledge, and thus may underestimate the total amount of knowledge produced by statistical learning. Indirect measures may be more sensitive indices of learning, capturing knowledge above and beyond what is reflected by recognition accuracy.

Auditory attention in childhood and adolescence: An event-related potential study of spatial selective attention to one of two simultaneous stories.

Auditory selective attention is a critical skill for goal-directed behavior, especially where noisy distractions may impede focusing attention. To better understand the developmental trajectory of auditory spatial selective attention in an acoustically complex environment, in the current study we measured auditory event-related potentials (ERPs) across five age groups: 3-5 years; 10 years; 13 years; 16 years; and young adults. Using a naturalistic dichotic listening paradigm, we characterized the ERP morphology for nonlinguistic and linguistic auditory probes embedded in attended and unattended stories. We documented robust maturational changes in auditory evoked potentials that were specific to the types of probes. Furthermore, we found a remarkable interplay between age and attention-modulation of auditory evoked potentials in terms of morphology and latency from the early years of childhood through young adulthood. The results are consistent with the view that attention can operate across age groups by modulating the amplitude of maturing auditory early-latency evoked potentials or by invoking later endogenous attention processes. Development of these processes is not uniform for probes with different acoustic properties within our acoustically dense speech-based dichotic listening task. In light of the developmental differences we demonstrate, researchers conducting future attention studies of children and adolescents should be wary of combining analyses across diverse ages.

Early auditory evoked potential is modulated by selective attention and related to individual differences in visual working memory capacity.

A growing body of research suggests that the predictive power of working memory (WM) capacity for measures of intellectual aptitude is due to the ability to control attention and select relevant information. Crucially, attentional mechanisms implicated in controlling access to WM are assumed to be domain-general, yet reports of enhanced attentional abilities in individuals with larger WM capacities are primarily within the visual domain. Here, we directly test the link between WM capacity and early attentional gating across sensory domains, hypothesizing that measures of visual WM capacity should predict an individual's capacity to allocate auditory selective attention. To address this question, auditory ERPs were recorded in a linguistic dichotic listening task, and individual differences in ERP modulations by attention were correlated with estimates of WM capacity obtained in a separate visual change detection task. Auditory selective attention enhanced ERP amplitudes at an early latency (ca. 70-90 msec), with larger P1 components elicited by linguistic probes embedded in an attended narrative. Moreover, this effect was associated with greater individual estimates of visual WM capacity. These findings support the view that domain-general attentional control mechanisms underlie the wide variation of WM capacity across individuals.

Enhanced peripheral visual processing in congenitally deaf humans is supported by multiple brain regions, including primary auditory cortex.

Brain reorganization associated with altered sensory experience clarifies the critical role of neuroplasticity in development. An example is enhanced peripheral visual processing associated with congenital deafness, but the neural systems supporting this have not been fully characterized. A gap in our understanding of deafness-enhanced peripheral vision is the contribution of primary auditory cortex. Previous studies of auditory cortex that use anatomical normalization across participants were limited by inter-subject variability of Heschl's gyrus. In addition to reorganized auditory cortex (cross-modal plasticity), a second gap in our understanding is the contribution of altered modality-specific cortices (visual intramodal plasticity in this case), as well as supramodal and multisensory cortices, especially when target detection is required across contrasts. Here we address these gaps by comparing fMRI signal change for peripheral vs. perifoveal visual stimulation (11-15° vs. 2-7°) in congenitally deaf and hearing participants in a blocked experimental design with two analytical approaches: a Heschl's gyrus region of interest analysis and a whole brain analysis. Our results using individually-defined primary auditory cortex (Heschl's gyrus) indicate that fMRI signal change for more peripheral stimuli was greater than perifoveal in deaf but not in hearing participants. Whole-brain analyses revealed differences between deaf and hearing participants for peripheral vs. perifoveal visual processing in extrastriate visual cortex including primary auditory cortex, MT+/V5, superior-temporal auditory, and multisensory and/or supramodal regions, such as posterior parietal cortex (PPC), frontal eye fields, anterior cingulate, and supplementary eye fields. Overall, these data demonstrate the contribution of neuroplasticity in multiple systems including primary auditory cortex, supramodal, and multisensory regions, to altered visual processing in congenitally deaf adults.

ERPs recorded during early second language exposure predict syntactic learning.

Millions of adults worldwide are faced with the task of learning a second language (L2). Understanding the neural mechanisms that support this learning process is an important area of scientific inquiry. However, most previous studies on the neural mechanisms underlying L2 acquisition have focused on characterizing the results of learning, relying upon end-state outcome measures in which learning is assessed after it has occurred, rather than on the learning process itself. In this study, we adopted a novel and more direct approach to investigate neural mechanisms engaged during L2 learning, in which we recorded ERPs from beginning adult learners as they were exposed to an unfamiliar L2 for the first time. Learners' proficiency in the L2 was then assessed behaviorally using a grammaticality judgment task, and ERP data acquired during initial L2 exposure were sorted as a function of performance on this task. High-proficiency learners showed a larger N100 effect to open-class content words compared with closed-class function words, whereas low-proficiency learners did not show a significant N100 difference between open- and closed-class words. In contrast, amplitude of the N400 word category effect correlated with learners' L2 comprehension, rather than predicting syntactic learning. Taken together, these results indicate that learners who spontaneously direct greater attention to open- rather than closed-class words when processing L2 input show better syntactic learning, suggesting a link between selective attention to open-class content words and acquisition of basic morphosyntactic rules. These findings highlight the importance of selective attention mechanisms for L2 acquisition.

Family-based training program improves brain function, cognition, and behavior in lower socioeconomic status preschoolers.

Using information from research on the neuroplasticity of selective attention and on the central role of successful parenting in child development, we developed and rigorously assessed a family-based training program designed to improve brain systems for selective attention in preschool children. One hundred forty-one lower socioeconomic status preschoolers enrolled in a Head Start program were randomly assigned to the training program, Head Start alone, or an active control group. Electrophysiological measures of children's brain functions supporting selective attention, standardized measures of cognition, and parent-reported child behaviors all favored children in the treatment program relative to both control groups. Positive changes were also observed in the parents themselves. Effect sizes ranged from one-quarter to half of a standard deviation. These results lend impetus to the further development and broader implementation of evidence-based education programs that target at-risk families.

The human brain processes syntax in the absence of conscious awareness.

Syntax is the core computational component of language. A longstanding idea about syntactic processing is that it is generally not available to conscious access, operating autonomously and automatically. However, there is little direct neurocognitive evidence on this issue. By measuring event-related potentials while human observers performed a novel cross-modal distraction task, we demonstrated that syntactic violations that were not consciously detected nonetheless produced a characteristic early neural response pattern, and also significantly delayed reaction times to a concurrent task. This early neural response was distinct from later neural activity that was observed only to syntactic violations that were consciously detected. These findings provide direct evidence that the human brain reacts to violations of syntax even when these violations are not consciously detected, indicating that even highly complex computational processes such as syntactic processing can occur outside the narrow window of conscious awareness.

Altered cross-modal processing in the primary auditory cortex of congenitally deaf adults: a visual-somatosensory fMRI study with a double-flash illusion.

The developing brain responds to the environment by using statistical correlations in input to guide functional and structural changes-that is, the brain displays neuroplasticity. Experience shapes brain development throughout life, but neuroplasticity is variable from one brain system to another. How does the early loss of a sensory modality affect this complex process? We examined cross-modal neuroplasticity in anatomically defined subregions of Heschl's gyrus, the site of human primary auditory cortex, in congenitally deaf humans by measuring the fMRI signal change in response to spatially coregistered visual, somatosensory, and bimodal stimuli. In the deaf Heschl's gyrus, signal change was greater for somatosensory and bimodal stimuli than that of hearing participants. Visual responses in Heschl's gyrus, larger in deaf than hearing, were smaller than those elicited by somatosensory stimulation. In contrast to Heschl's gyrus, in the superior-temporal cortex visual signal was comparable to somatosensory signal. In addition, deaf adults perceived bimodal stimuli differently; in contrast to hearing adults, they were susceptible to a double-flash visual illusion induced by two touches to the face. Somatosensory and bimodal signal change in rostrolateral Heschl's gyrus predicted the strength of the visual illusion in the deaf adults in line with the interpretation that the illusion is a functional consequence of the altered cross-modal organization observed in deaf auditory cortex. Our results demonstrate that congenital and profound deafness alters how vision and somatosensation are processed in primary auditory cortex.

The influence of language proficiency on lexical semantic processing in native and late learners of English.

We investigated the influence of English proficiency on ERPs elicited by lexical semantic violations in English sentences, in both native English speakers and native Spanish speakers who learned English in adulthood. All participants were administered a standardized test of English proficiency, and data were analyzed using linear mixed effects (LME) modeling. Relative to native learners, late learners showed reduced amplitude and delayed onset of the N400 component associated with reading semantic violations. As well, after the N400 late learners showed reduced anterior negative scalp potentials and increased posterior potentials. In both native and late learners, N400 amplitudes to semantically appropriate words were larger for people with lower English proficiency. N400 amplitudes to semantic violations, however, were not influenced by proficiency. Although both N400 onset latency and the late ERP effects differed between L1 and L2 learners, neither correlated with proficiency. Different approaches to dealing with the high degree of correlation between proficiency and native/late learner group status are discussed in the context of LME modeling. The results thus indicate that proficiency can modulate ERP effects in both L1 and L2 learners, and for some measures (in this case, N400 amplitude), L1-L2 differences may be entirely accounted for by proficiency. On the other hand, not all effects of L2 learning can be attributed to proficiency. Rather, the differences in N400 onset and the post-N400 violation effects appear to reflect fundamental differences in L1-L2 processing.

Emergence of the neural network for reading in five-year-old beginning readers of different levels of pre-literacy abilities: an fMRI study.

The present study traced the emergence of the neural circuits for reading in five-year-old children of diverse pre-literacy ability. In the fall and winter of kindergarten, children performed a one-back task with letter versus false font stimuli during fMRI scanning. At the start of kindergarten, children with on-track pre-literacy skills (OT) recruited bilateral temporo-parietal regions for the letter > false font comparison. In contrast, children at-risk for reading difficulty (AR) showed no differential activation in this region. Following 3 months of kindergarten and, for AR children, supplemental reading instruction, OT children showed left-lateralized activation in the temporo-parietal region, whereas AR children showed bilateral activation and recruitment of frontal regions including the anterior cingulate cortex. These data suggest that typical reading development is associated with initial recruitment and subsequent disengagement of right hemisphere homologous regions while atypical reading development may be associated with compensatory recruitment of frontal regions.

Maturational constraints on the recruitment of early processes for syntactic processing.

An enduring question in the study of second-language acquisition concerns the relative contributions of age of acquisition (AOA) and ultimate linguistic proficiency to neural organization for second-language processing. Several ERP and neuroimaging studies of second-language learners have found that neural organization for syntactic processing is sensitive to delays in second-language acquisition. However, such delays in second-language acquisition are typically associated with lower language proficiency, rendering it difficult to assess whether differences in AOA or proficiency lead to these effects. Here we examined the effects of delayed second-language acquisition while controlling for proficiency differences by examining participants who differ in AOA but who were matched for proficiency in the same language. We compared the ERP response to auditory English phrase structure violations in a group of late learners of English matched for grammatical proficiency with a group of English native speakers. In the native speaker group, violations elicited a bilateral and prolonged anterior negativity, with onset at 100 msec, followed by a posterior positivity (P600). In contrast, in the nonnative speaker group, violations did not elicit the early anterior negativity, but did elicit a P600 which was more widespread spatially and temporally than that of the native speaker group. These results suggest that neural organization for syntactic processing is sensitive to delays in language acquisition independently of proficiency level. More specifically, they suggest that both early and later syntactic processes are sensitive to maturational constraints. These results also suggest that late learners who reach a high level of second-language proficiency rely on different neural mechanisms than native speakers of that language.