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Healthy and Abnormal Development of the Prefrontal Cortex

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Healthy and Abnormal Development of the Prefrontal Cortex Developmental Neurorehabilitation, October 2009; 12(5): 279–297 Healthy and abnormal development of the prefrontal cortex MEGAN SPENCER-SMITH1,2 & VICKI ANDERSON1,2,3 1Murdoch Childrens Research Institute, Melbourne, Australia, 2University of Melbourne, Melbourne, Australia, and 3Royal Children’s Hospital, Melbourne, Australia (Received 8 October 2008; accepted 3 June 2009) Abstract Background: While many children with brain conditions present with cognitive, behavioural, emotional, academic and social impairments, other children recover with seemingly few impairments. Animal studies and preliminary child studies have identified timing of brain lesion as a key predictor in determining functional outcome following early brain lesions. Review: This research suggests that knowledge of healthy developmental processes in brain structure and function is essential for better understanding functional recovery and outcome in children with brain lesions. This review paper aims to equip researchers with current knowledge of key principles of developmental processes in brain structure and function. Timetables for development of the prefrontal cortex (PFC), a brain region particularly vulnerable to lesions due to its protracted developmental course, are examined. In addition, timetables for development of executive skills, which emerge in childhood and have a prolonged developmental course that parallels development of the PFC, are also discussed. Conclusions: Equipped with this knowledge, researchers are now in a better position to understand functional recovery and outcome in children with brain conditions. Keywords: Development, prefrontal cortex, executive functions, brain injury Introduction are clearly determined by a complex and constantly For personal use only. changing relationship with all of these factors. Many children with brain conditions present with Timing of brain lesion has been identified as a cognitive, behavioural, emotional, academic and central predictor of functional outcome in animal social impairments, often requiring lifetime inter- focal lesion studies [21–24] and preliminary child vention and support. Some children, however, studies [4,11]. Key principles that have emerged demonstrate considerable recovery and seemingly from this research suggest that developmental pro- few impairments. Research attempting to under- stand this variance has focused on identifying cesses occurring at the time of the brain lesion are predictors of outcome in groups of children with particularly vulnerable to disruption. Further, these specific brain conditions, such as traumatic brain studies suggest that aetiology of the brain condition may be only one of many factors that shape Dev Neurorehabil Downloaded from informahealthcare.com by Yeshiva University on 03/03/13 injury [1,2], focal brain injury [3–6], cerebral toxicity and childhood cancers [7–10], stroke [11], cerebral functional outcomes. Based on systematic studies infection [12,13], seizures [14–17], metabolic dis- of focal frontal lesions in rats, Kolb et al. [25] turbance [18,19] and prematurity [20]. Together propose critical periods in rat neurological develop- these studies are building a picture demonstrating ment when brain lesions are associated with poor or the capacity of the immature brain to recover and better functional outcome and further suggest these develop after a brain lesion. These studies also critical periods may extrapolate to humans. While suggest that outcome is related to identifiable brain human research provides preliminary support for lesion characteristics as well as developmental, these critical periods, the model has not yet been environmental and constitutional factors. systematically examined to determine whether it Individually these factors do not adequately explain applies to humans. Based on child and adult studies the variance in outcome observed in children with examining language outcome after brain injury, brain conditions. Functional recovery and outcome Dennis [26] proposed stages in skill maturation Correspondence: Megan Spencer-Smith, Critical Care and Neurosciences, Murdoch Childrens Research Institute, Royal Children’s Hospital, Flemington Road, Parkville, VIC 3054, Australia. Tel: þ61 3 9090 5253. Fax: +61 3 9090 5212. E-mail: [email protected] ISSN 1751–8423 print/ISSN 1751–8431 online/09/050279–19 ß 2009 Informa UK Ltd. DOI: 10.1080/17518420903090701 280 M. Spencer-Smith & V. Anderson when injury will be associated with poor or better cortical regions, connected via specific neural cir- outcome for that skill. This heuristic, however, has cuits [30,31]. Lesion studies and functional imaging not yet been empirically tested to determine whether studies demonstrate that separate frontal regions its principles extend to other cognitive skills. support specific cognitive processes. For example, Considerable research and theory has been direc- the medial prefrontal region has been shown to ted towards better understanding the development support attentional control processes including of structural and functional specificity through focused attention [32] and self-regulation [28]. childhood. Early studies argued strongly for innate Some evidence challenges this modular approach specialization of the brain [27], however more [33–35]. Stuss [35] has reported executive dysfunc- contemporary studies are accumulating that suggest tion in adults after extra-frontal brain damage and regions in the developing brain may not be as func- interpreted these findings as evidence that EF are tionally specific as those in the mature brain [28,29]. associated with complex frontal and extra-frontal Accordingly, damage to the developing brain, when systems. While the PFC is critical for EF, it appears brain networks are less established and therefore that integrity of the whole brain may be necessary for more brain regions are recruited to perform tasks, efficient EF [36–38]. This is especially the case in may result in more generalized dysfunction. the developing brain, which has less established Alternatively, reduced localization of function may connectivity and structure. allow for compensation or development of new How and when the brain becomes specialized is networks in the context of brain lesion. In order to particularly relevant to understanding the neurobe- determine when greater or less potential for recovery havioural consequences of brain lesions. Early might occur in children with brain conditions, researchers suggested contradicting possibilities. knowledge of healthy brain development is essential. Lenneberg [39] argued that the infant’s brain was This paper outlines healthy processes in develop- ‘equipotential’ and that functional specialization ment of brain structure and function that are emerged gradually through early childhood. essential for understanding functional outcomes in In contrast, the ‘innate specialization’ model argues children with brain conditions. General principles of that key skills such as language are localized at birth brain development that are helpful for understating [27]. More contemporary research examining the mature brain are discussed. A review of time- human functional brain development highlights the tables for key neurological processes in development importance of accounting for the influence of expe- of the prefrontal cortex (PFC) is presented. This rience and genetics on the developing organisation of For personal use only. brain region is especially vulnerable to brain lesions the brain. Johnson [30,40] acknowledges these due to its extended developmental trajectory. influences and identifies three separate, but not Research shows that, in adults, executive functions necessarily incompatible, approaches to understand- (EF) rely strongly on the integrity of the PFC, which ing progression of cognitive abilities in infants: (a) plays an important role in efficient EF. Therefore, maturation; (b) interactive specialization; and (c) skill timetables for development of executive skills are learning. also outlined and parallels in development of brain The maturational view proposes that the develop- structure and function are examined. This review mental sequence of specific neuroanatomical regions aims to provide an understanding of functional enables the hierarchical emergence of sensory, motor outcome in children with brain conditions. and cognitive processes. For example, the dorso- Dev Neurorehabil Downloaded from informahealthcare.com by Yeshiva University on 03/03/13 lateral PFC (DL-PFC) supports successful perfor- mance on the object retrieval task, designed to assess Healthy brain development working memory and inhibitory control in children [41]. Successful performance on the task involves While there is some understanding about healthy activation of several brain regions, but the particu- brain development, the impact of brain lesions on larly protracted development of the DL-PFC is the expected course of development is unknown. thought to be primarily responsible for change in Knowledge of how and when the brain becomes behaviour, limiting the child’s efficiency until these specialized, leading to its mature state, assists in brain regions are mature. understanding and investigation of functional and The interactive specialization view suggests that structural consequences of brain lesions. emergence of a new skill reflects refinement of connectivity between brain regions and not just Theories of human functional brain development activity in one or more region.
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