Puberty contributes to adolescent development of fronto-striatal functional connectivity supporting inhibitory control

Ojha, Amar; Parr, Ashley C.; Foran, Will; Calabro, Finnegan J.; Luna, Beatríz

doi:10.1016/j.dcn.2022.101183

Cited by 15 publications

(8 citation statements)

References 106 publications

(146 reference statements)

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“…Whilst white matter volumes increase throughout adolescence in both sexes, this process occurs more rapidly in adolescent males resulting in an increasing magnitude of sex differences. 31 The role of puberty vs chronological age in neurodevelopment in adolescence Hormonal changes in puberty are not just responsible for the development of physical secondary sex characteristics, they also drive many of the neurodevelopmental changes in the adolescent brain described above, particularly with respect to the development of frontal cortical circuits, and hippocampal and amygdala connectivity 7,[32][33][34][35] . In a functional MRI study of 105, 8-19 year olds, Ravindranath et al found that whilst chronological age was associated with activations in the right dorsolateral prefrontal cortex on a task requiring inhibitory control, puberty stage was associated with activation in the right ventrolateral prefrontal cortex.…”

Section: Adolescence: a Critical Period For Synaptic Pruning And Myel...mentioning

confidence: 99%

The Impact of Suppressing Puberty on Neuropsychological Function

Baxendale

2024

Preprint

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Concerns have been raised regarding the neuropsychological impact of medications that interrupt puberty, given the magnitude and complexity of changes that occur in brain function and structure during this sensitive window of neurodevelopment. This review examines the literature on the impact of pubertal suppression on cognitive and behavioural function in animals and humans. In mammals the effects are complex and often sex specific. There is no evidence that cognitive effects are fully reversible following discontinuation of treatment. No human studies have systematically explored the impact of these treatments on neuropsychological function with an adequate baseline and follow up. However there is some evidence of a detrimental impact of pubertal suppression on IQ, concordant with findings in the wider literature on gonadotropin-hormonereleasing-hormone expression in relevant brain structures. Critical questions remain unanswered regarding the nature, extent and permanence of any arrested development of cognitive function that may be associated with pharmacological blocking of puberty in humans. The impact of puberal suppression on measures of neuropsychological functions should be an urgent priority for future research. Neuropsychologists should be an integral member of the multidisciplinary team caring for people treated with puberty blockers to monitor the impact of these treatments.

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Section: Adolescence: a Critical Period For Synaptic Pruning And Myel...mentioning

confidence: 99%

The Impact of Suppressing Puberty on Neuropsychological Function

Baxendale

2024

Preprint

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“…Centered on the caudate, putamen, and nucleus accumbens, the network is highly connected to the prefrontal cortex, the amygdala, and the hippocampus (Guyer et al, 2006;Nelson et al, 2016). Puberty-related maturation of fronto-striatal functional connectivity has been linked to inhibitory control development (Ojha et al, 2022).…”

Section: Second Hit: Adolescencementioning

confidence: 99%

A two-hit model of behavioral inhibition and anxiety

Ostlund¹,

Pérez‐Edgar²

2023

Preprint

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Four decades of research has examined the antecedents and consequences of behavioral inhibition (BI), a temperament profile associated with heightened reactivity to sensory stimuli in infancy, reticence towards social cues in childhood, and the later emergence of social anxiety in adolescence. This review proposes that a two-hit model can supplement prior work to better understand these developmental pathways. Specifically, time limited experiences (“hits”) centered in infancy and adolescence stress idiosyncratic BI-linked processes that uniquely trigger the developmental pathway from temperament to disorder. To illustrate, we focus on caregiver distress in infancy (including fetal development) and social reorientation in adolescence, and the impact on malleable attentional and cognitive systems. These are developmental challenges and processes that go to the heart of the BI phenotype. Finally, we note open questions in this conceptual model, potential caveats, and needed future research.

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“…Altered connectivity within these fronto-striatal circuits has been linked to a range of psychiatric disorders (Burguière, Monteiro, Mallet, Feng, & Graybiel, 2015;Furman, Hamilton, & Gotlib, 2011;Kim et al, 2019;Morein-Zamir & Robbins, 2015). The dorsal fronto-striatal system includes connections between the dorsolateral prefrontal cortex (dlPFC) and the dorsal striatum, consisting of the caudate and putamen (Alexander et al, 1986;Morris et al, 2016), and is thought to mediate cognitive processes such as inhibitory control, goal-directed behavior, reward responsivity, and cognitive flexibility, that are potentially clinically relevant in AN (Grahn, Parkinson, & Owen, 2008;Ojha, Parr, Foran, Calabro, & Luna, 2022;Staudinger, Erk, & Walter, 2011;Vaghi et al, 2017). Indeed, findings from MRI studies provide converging evidence of abnormalities within dorsal fronto-striatal regions among patients with AN, both structurally and across a variety of tasks (Foerde et al, 2020;Foerde, Steinglass, Shohamy, & Walsh, 2015;Foerde et al, 2021;Frank, Shott, Hagman, & Mittal, 2013;Friederich et al, 2012;Martin Monzon et al, 2017;Sanders et al, 2015;Titova, Hjorth, Schiöth, & Brooks, 2013;Zhu et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

Reduced dorsal fronto-striatal connectivity at rest in anorexia nervosa

Muratore,

Foerde,

Lloyd

et al. 2024

Psychol. Med.

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Background Anorexia nervosa (AN) is a serious psychiatric illness that remains difficult to treat. Elucidating the neural mechanisms of AN is necessary to identify novel treatment targets and improve outcomes. A growing body of literature points to a role for dorsal fronto-striatal circuitry in the pathophysiology of AN, with increasing evidence of abnormal task-based fMRI activation within this network among patients with AN. Whether these abnormalities are present at rest and reflect fundamental differences in brain organization is unclear. Methods The current study combined resting-state fMRI data from patients with AN (n = 89) and healthy controls (HC; n = 92) across four studies, removing site effects using ComBat harmonization. First, the a priori hypothesis that dorsal fronto-striatal connectivity strength – specifically between the anterior caudate and dlPFC – differed between patients and HC was tested using seed-based functional connectivity analysis with small-volume correction. To assess specificity of effects, exploratory analyses examined anterior caudate whole-brain connectivity, amplitude of low-frequency fluctuations (ALFF), and node centrality. Results Compared to HC, patients showed significantly reduced right, but not left, anterior caudate-dlPFC connectivity (p = 0.002) in small-volume corrected analyses. Whole-brain analyses also identified reduced connectivity between the right anterior caudate and left superior frontal and middle frontal gyri (p = 0.028) and increased connectivity between the right anterior caudate and right occipital cortex (p = 0.038). No group differences were found in analyses of anterior caudate ALFF and node centrality. Conclusions Decreased coupling of dorsal fronto-striatal regions indicates that circuit-based abnormalities persist at rest and suggests this network may be a potential treatment target.

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Puberty contributes to adolescent development of fronto-striatal functional connectivity supporting inhibitory control

Cited by 15 publications

References 106 publications

The Impact of Suppressing Puberty on Neuropsychological Function

The Impact of Suppressing Puberty on Neuropsychological Function

A two-hit model of behavioral inhibition and anxiety

Reduced dorsal fronto-striatal connectivity at rest in anorexia nervosa

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