Implications of age at lesion onset for neuropsychological outcomes: A systematic review focusing on focal brain lesions

Sullivan, Alyssa W; Johnson, Marcie King; Boes, Aaron D.; Tranel, Daniel

doi:10.1016/j.cortex.2023.03.002

Cited by 4 publications

(1 citation statement)

References 131 publications

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“…This could indicate that, if the epilepsy emerges early in the still-maturing brain, it could impact on cognitive development disproportionally. 66 Independently of this effect of age of epilepsy onset, we found that a longer duration of epilepsy further impacted negatively upon neuropsychological abilities, calling for early intervention.…”

Section: Discussionmentioning

confidence: 74%

Long-term neuropsychological trajectories in children with epilepsy: does surgery halt decline?

Eriksson,

Prentice,

Piper

et al. 2024

Brain

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Neuropsychological impairments are common in children with drug-resistant epilepsy. It has been proposed that epilepsy surgery may alleviate these impairments by providing seizure freedom; however, findings from prior studies have been inconsistent. We mapped long-term neuropsychological trajectories in children before and after undergoing epilepsy surgery, to measure the impact of disease course and surgery on functioning. We performed a retrospective cohort study of 882 children who had undergone epilepsy surgery at Great Ormond Street Hospital (1990-2018). We extracted patient information and neuropsychological functioning – obtained from IQ tests (domains: Full-Scale IQ, Verbal IQ, Performance IQ, Working Memory, and Processing Speed) and tests of academic attainment (Reading, Spelling and Numeracy) – and investigated changes in functioning using regression analyses. We identified 500 children (248 females) who had undergone epilepsy surgery (median age at surgery = 11.9 years, interquartile range = [7.8,15.0]) and neuropsychology assessment. These children showed declines in all domains of neuropsychological functioning in the time leading up to surgery (all p-values ≤ 0.001; e.g., βFSIQ = -1.9, SEFSIQ = 0.3, pFSIQ < 0.001). Children lost on average one to four points per year, depending on the domain considered; 27-43% declined by 10 or more points from their first to their last preoperative assessment. At the time of presurgical evaluation, most children (46-60%) scored one or more standard deviations below the mean (<85) on the different neuropsychological domains; 37% of these met the threshold for intellectual disability (Full-Scale IQ < 70). On a group level, there was no change in performance from pre- to postoperative assessment on any of the domains (all p-values > 0.128). However, children who became seizure-free through surgery showed higher postoperative neuropsychological performance (e.g., rrb-FSIQ = 0.37, p < 0.001). These children continued to demonstrate improvements in neuropsychological functioning over the course of their long-term follow-up (e.g., βFSIQ = 0.9, SEFSIQ = 0.3, pFSIQ = 0.004). Children who had discontinued antiseizure medication (ASM) treatment at one-year follow-up showed an eight-to-13-point advantage in postoperative Working Memory, Processing Speed, and Numeracy, and greater improvements in Verbal IQ, Working Memory, Reading, and Spelling (all p-values < 0.034) over the postoperative period compared to children who were seizure-free and still receiving ASMs. In conclusion, by providing seizure freedom and the opportunity for ASM cessation, epilepsy surgery may not only halt but reverse the downward trajectory that children with drug-resistant epilepsy display in neuropsychological functioning. To halt this decline as soon as possible, or potentially prevent it from occurring in the first place, children with focal epilepsy should be considered for epilepsy surgery as early as possible after diagnosis.

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Section: Discussionmentioning

confidence: 74%

Long-term neuropsychological trajectories in children with epilepsy: does surgery halt decline?

Eriksson,

Prentice,

Piper

et al. 2024

Brain

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Behavioral and anatomical effects of complex rearing after day 7 neonatal frontal lesions vary with sex

Gibb,

Kolb

2024

Preprint

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Rats received medial frontal lesions, or sham surgery, on postnatal day 7 (P7), and were placed in complex environments or standard lab housing at weaning. Three months later the animals were tested in a spatial learning task and in a skilled reaching task. Rats with P7 lesions had smaller deficits in spatial learning than similar adult operates, and males performed better than females. Complex housing further improved the performance of male, but not female, lesion rats. The opposite was seen in motor performance as female lesion rats performed better than males and benefited from experience whereas males did not. There was a correlation between behavior and dendritic change as complex housing reversed lesion-induced dendritic atrophy, an effect that was greater in males. P7 frontal males, but not females, showed an increase in spine density that was reversed by complex housing. Experience thus can affect functional and anatomical outcome after early brain injury, but the effects vary with sex.

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Brain growth until adolescence after a neonatal focal injury: sex related differences beyond lesion effect

Postic,

Leprince,

Brosset

et al. 2024

Front. Neurosci.

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IntroductionEarly focal brain injuries lead to long-term disabilities with frequent cognitive impairments, suggesting global dysfunction beyond the lesion. While plasticity of the immature brain promotes better learning, outcome variability across individuals is multifactorial. Males are more vulnerable to early injuries and neurodevelopmental disorders than females, but long-term sex differences in brain growth after an early focal lesion have not been described yet. With this MRI longitudinal morphometry study of brain development after a Neonatal Arterial Ischemic Stroke (NAIS), we searched for differences between males and females in the trajectories of ipsi- and contralesional gray matter growth in childhood and adolescence, while accounting for lesion characteristics.MethodsWe relied on a longitudinal cohort (AVCnn) of patients with unilateral NAIS who underwent clinical and MRI assessments at ages 7 and 16 were compared to age-matched controls. Non-lesioned volumes of gray matter (hemispheres, lobes, regions, deep structures, cerebellum) were extracted from segmented T1 MRI images at 7 (Patients: 23 M, 16 F; Controls: 17 M, 18 F) and 16 (Patients: 18 M, 11 F; Controls: 16 M, 15 F). These volumes were analyzed using a Linear Mixed Model accounting for age, sex, and lesion characteristics.ResultsWhole hemisphere volumes were reduced at both ages in patients compared to controls (gray matter volume: −16% in males, −10% in females). In ipsilesional hemisphere, cortical gray matter and thalamic volume losses (average −13%) mostly depended on lesion severity, suggesting diaschisis, with minimal effect of patient sex. In the contralesional hemisphere however, we consistently found sex differences in gray matter volumes, as only male volumes were smaller than in male controls (average −7.5%), mostly in territories mirroring the contralateral lesion. Females did not significantly deviate from the typical trajectories of female controls. Similar sex differences were found in both cerebellar hemispheres.DiscussionThese results suggest sex-dependent growth trajectories after an early brain lesion with a contralesional growth deficit in males only. The similarity of patterns at ages 7 and 16 suggests that puberty has little effect on these trajectories, and that most of the deviation in males occurs in early childhood, in line with the well-described perinatal vulnerability of the male brain, and with no compensation thereafter.

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Implications of age at lesion onset for neuropsychological outcomes: A systematic review focusing on focal brain lesions

Cited by 4 publications

References 131 publications

Long-term neuropsychological trajectories in children with epilepsy: does surgery halt decline?

Long-term neuropsychological trajectories in children with epilepsy: does surgery halt decline?

Behavioral and anatomical effects of complex rearing after day 7 neonatal frontal lesions vary with sex

Brain growth until adolescence after a neonatal focal injury: sex related differences beyond lesion effect

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