Findings from this neuroimaging study are consistent with our hypothesis that prematurity is a modulator of the neural response to increased task demands (here, increased sentence length or syntactic difficulty) during auditory sentence comprehension. Adolescent participants completed an auditory sentence verification task in the fMRI scanner, a task that entailed listening to a sentence, viewing a picture, and pressing a button to indicated whether or not the picture accurately depicted the meaning of the sentence. Two factors, sentence length and syntactic difficulty, were manipulated in a factorial design and we analyzed two phases within each trial. The Auditory phase reflected participants’ ability to passively listen to and comprehend the sentences, while the Verification/Response phase necessitated higher-order cognition, i.e., comparing the meaning of the sentence to a visual image and making a decision as to its validity. Accuracy and response time during the task were reasonably similar between groups. Critically, ANOVA tests of the areas of neural activation demonstrated no main effects of group, but rather several interesting group by condition interactions. Children born preterm showed important differences in response to increased task demands compared to children born at term, even when performance on the task was comparable.
A particular strength of the design was that both preterm and full term adolescents had scores on standardized assessments of IQ, receptive vocabulary, and receptive language skill that were within normal limits, and scores on these measures were also reasonably well matched between groups prior to scanning. In this way, differences between groups can reliably be attributed to prematurity and not to differential performance.
4.3 Interactions in the Auditory phase
During the Auditory phase of the task, the significant group × length interaction activated left and right superior temporal gyrus and the occipital lobe. Longer sentences also activated similar regions in our previous study (Yeatman et al., 2010
); likely reflecting increased auditory, linguistic, and semantic processing. Examination of image data extracted from the three significant clusters in the interaction (see , Panel B) indicates that preterms showed numerically larger differences between longer and shorter sentences relative to full terms; the greater activation perhaps suggesting greater cognitive output to meet task demands. Post hoc
tests revealed that the length manipulation elicited a significantly greater activation in full terms relative to preterms in left and right occipital lobes, and left medial frontal gyrus. Medial frontal gyrus activation has previously been observed in neuroimaging studies of sentence comprehension, particularly when sentences included subject- and object-relative clauses (Caplan et al., 1999
; Caplan et al., 2000
) as did our sentences. Caplan and colleagues tentatively attributed activation in medial frontal gyri to roles in attentional and control processes (Posner et al., 1987
). Thus, the post hoc
findings for the full term group suggest that they appropriately recruit areas of the brain in the initial phase of the task that support other cognitive mechanisms (i.e., attention, cognitive control) to handle increased task demands.
4.4. Interactions in the Verification/Response phase
Turning to the Verification/Response phase of the trial, the significant interactions showed wider activation patterns than earlier in the trial, reflecting the change in cognitive demands from passive listening to active verification and formulation of a response. We again found a group × length interaction in this later phase, and most of this activation was left-lateralized. Beyond the right and left superior and middle temporal gyri and left occipital lobe activation related to increased sentence length that we found in the Auditory phase, we also observed activation in left middle frontal gyrus, left inferior frontal gyrus, the left precuneus, and the postcentral gyrus in the left hemisphere. Moreover, examination of the image data for each of these significant clusters in the interaction, as well as post hoc
tests, point to large differences between preterm and full term groups in the left frontal regions and the left precuneus. Activation in these clusters is consistent with other fMRI studies of sentence comprehension/verification tasks that reported activation in Broca’s area and left prefrontal cortex more generally (Bunge et al., 2000
; Hashimoto & Sakai, 2002
; Rogalsky & Hickok, 2011
), as well as the left temporal lobe (Friederici, 2002
). It appears that preterms require greater recruitment of prefrontal cortex relative to their full term peers when verifying and responding to longer sentences. The precuneus has been implicated in tasks requiring visuospatial imagery and episodic retrieval (Cavanna et al., 2006
; Krause et al., 1999
; Lundstrom et al., 2005
), perhaps suggesting that preterms rely more on a visual imagery strategy than full term children when listening to longer sentences.
Importantly, we found a significant group × difficulty interaction in the second phase of the trial in left and right middle temporal gyrus, left precuneus, left insula, right cerebellum, and right cingulate gyrus. Interestingly, there was overlap between areas related to the interaction of group × length and group × difficulty; the common activation in bilateral superior temporal gyri and left precuneus areas suggests a shared system for accommodating increased task demands in sentence comprehension, though the two groups differentially recruited these areas of the brain. Last and most relevant to the aims of the study, post hoc
tests revealed that the difference in activation related to Difficult versus Easy sentences was greater for preterms relative to full terms in the left and right middle frontal gyri (a part of the dorsolateral prefrontal cortex). This finding suggests that in comparison to full term peers, preterm adolescents recruited areas of the brain associated with cognitive control (MacDonald et al., 2000
) when processing difficult material. We know that cognitive control is a domain that is weak in preterms as a group (Loe et al., 2011
). We carefully note that though speculative at this point, it is plausible that preterm children have to engage cognitive control mechanisms more than full term children in order to attain comparable performance in the scanner. Thus, underlying apparently normal performance may be different neural mechanisms, pointing to the continued need for more neuroimaging research to understand the functional differences in preterms on linguistic and cognitive tasks.
Taken together, these findings are notable for an absence of main effects of group collapsing across both task conditions (increased sentence length or syntactic difficulty). Instead, we found group × condition interactions: in both phases of the trial we found a group × length interaction, and in the second phase of the trial we found a group × difficulty interaction. Moreover, post hoc tests of both interactions in the second phase of the trial, where participants verified the relationship between sentence and picture and made a YES/NO response, revealed that the preterm group had greater activation in response to the experimental contrasts relative to the full terms, but not vice versa. The single most important take-home message from these findings is that group status (i.e., presence/absence of preterm birth) modulated the functional neuroanatomy related to increased task demands during auditory sentence comprehension. We verified that through ANCOVA analyses that the group differences could not be attributed to any subtle between-group differences in age, receptive language skill, or reaction time in the scanner.
4.5 Educational implications
There has been an intense debate regarding the integration of cognitive neuroscience and education (Blakemore & Frith, 2005
; Gabrieli, 2009
; Goswami, 2006
; Howard-Jones, 2010
; Varma et al., 2008
). Translating brain-behavior findings directly into meaningful changes in curricula or into best practices within the educational system is an endeavor that some believe at best should be attempted cautiously (Bruer, 1997
; Goswami, 2009
; Stern, 2005
). We agree that neuroscience at this point in time cannot readily inform the development of educational curricular or teaching methods. For such purposes, behavioral and educational research provides a more direct approach for assessment of whether a particular curriculum or teaching method is effective.
Yet cognitive neuroscience has provided numerous findings from atypical populations that afforded points of reference between the disciplines and in turn shaped educational approaches, including reading/dyslexia (Frey & Fisher, 2010
; Gabrieli, 2009
; Hoeft et al., 2010; Kevan & Pammer, 2009
), mathematical learning/dyscalculia (Butterworth et al., 2011
), emotion regulation/behavioral disorders (Blair, 2002
; MacLeod, 2010
; Ochsner et al., 2010), and attention/ADHD (Loe et al., 2011
; Vaidya et al., 2005
). The contribution of cognitive neuroscience has focused on identifying both core deficits and underlying phenotypes of a particular disorder or deficit; these findings in turn have guided the creation of targeted interventions and development of evidence-based practices in education (Fletcher et al., 2005
; Räsänen et al., 2009
; Shaywitz et al., 2004
; Wilson et al., 2006
We believe that studies, such as this one, are similarly relevant to education because they provide important insights about the students, though not students with obvious impairments in an academic domain. Rather, this study informs us about intrinsic, background factors pertinent to education and optimal academic achievement. In a similar way, for example, drawing from research in literacy development, we know that poor readers from families with low SES show different patterns of activation than poor readers with high SES (Noble et al., 2006
), equating for performance on a reading-related task. This finding does not in and of itself determine which is the best curriculum for teaching reading to everyone, or even to poor children. However, it suggests that the way children process information for reading is the cumulative effect of their social history and circumstance. The educational implications of these findings are that literacy programs may need to consider the child’s SES in developing and assessing educational methods or in providing accommodations for children from poor homes. Also, intervention studies prompted by research like that of Noble and colleagues (2006)
may account for variation in extrinsic factors such as SES in the efficacy of their training programs (Keller & Just, 2009
; Meyler et al., 2008
In this study, we show that children born preterm who have performance comparable to full term peers have different patterns of neural activation on a language comprehension task. These effects persisted when variance in age, receptive language, and response time were taken into account. The engagement of regions of frontal lobe suggests that preterm children may be utilizing cognitive control areas to a greater degree in the late phase of the task than do their full term peers. If we agree that these findings suggest greater recruitment of cognitive control mechanisms among the preterm group, then we may need to consider strategies to reduce the need for effortful control processes when teaching and assessing children born preterm. Accommodations, such as more trials for learning, use of visual and other supports for understanding, and/or more time during testing, might be appropriate for this population.
We recognize that we have studied a small sample of children born preterm who may not be fully representative of the entire population. We recognize that we must validate methods, such as co-registration and normalization of the clinical and typical population together. We further acknowledge that the differences in neural activations that we found are modest in the Auditory Phase, where full terms showed greater activation on post hoc tests, and greater in the second phase of the task, where preterms showed greater activation on post hocs. However, we believe these observations open the door for a new type of inquiry into intrinsic variation among students on the basis of medical history, even students whose performance appears typical at the behavioral level.
We hope the findings in this paper inspire efforts toward better understanding of the neural basis of cognitive and linguistic ability for atypical populations of children. We emphasize this understanding of distinctive neural activation patterns is particularly important in cases where children with atypical medical histories and/or neurological status have comparable performance on standardized measures and do not meet eligibility for special education. How researchers in the fields of cognitive neuroscience and education should intervene differently is a matter for future study. Certainly the basic findings herein need to be replicated and extended to other linguistic, cognitive, and academic outcomes. In cases where students are not eligible for special education, future findings may guide mainstream classroom accommodations that collectively provide relief from the increased effort required to attain normal performance. Educational policy may also need to allow for variations in eligibility criteria as a function of medical and/or neurological history.