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Early-life medial pulvinar disruption drives schizophrenia-relevant prefrontal inhibitory and cognitive deficits in
Jack T Scott1, Sara Fin2, Adam P Caccavano3
1Section on Cellular and Cognitive Neurodevelopment, National Institute of Mental Health, National Institutes of Health; Bethesda, MD 20892, USA.
Insights
Damage to the medial pulvinar in infant marmosets disrupted prefrontal cortex development, causing lasting working memory deficits. This suggests thalamic input is crucial for early brain maturation and may underlie psychiatric disorders.
Area of Science:
- Neuroscience
- Developmental Neuroscience
- Primate Models
Background:
- Schizophrenia is linked to disrupted postnatal maturation of prefrontal circuits.
- The developmental trajectory from early vulnerability to adult cortical dysfunction is not fully understood.
Purpose of the Study:
- To investigate the role of the primate medial pulvinar in prefrontal cortex maturation.
- To determine if early-life medial pulvinar damage impacts adolescent and adult prefrontal function.
Main Methods:
- Bilateral medial pulvinar lesions were performed in neonatal marmosets.
- Diffusion imaging, working memory tests, electrophysiology, and immunohistochemistry were used to assess prefrontal cortex development and function.
Main Results:
- Neonatal lesions altered adolescent prefrontal diffusion trajectories.
- Adult marmosets with early lesions exhibited working memory deficits, unlike those lesioned in adulthood.
- Early lesions reduced thalamocortical input to interneurons, diminished gamma power, and revealed immature interneuron physiology.
Conclusions:
- Thalamic input during a critical developmental window shapes prefrontal inhibitory maturation.
- Dysfunction in thalamic inputs, not solely cortical issues, may contribute to psychiatric disorders like schizophrenia.
Abstract:
Schizophrenia is thought to arise from disrupted postnatal maturation of prefrontal circuits, but the developmental events linking early vulnerability to adult cortical dysfunction remain unclear. Here, we tested whether the primate medial pulvinar, a higher-order thalamic nucleus interconnected with prefrontal cortex, contributes to prefrontal maturation. Bilateral medial pulvinar lesions in neonatal marmosets altered adolescent prefrontal diffusion trajectories and produced adult working memory deficits, the latter of which did not follow comparable lesions in adulthood. Early-life lesioned animals showed reduced thalamocortical input to layer 3 parvalbumin interneurons, diminished prefrontal gamma power, reduced parvalbumin expression, and immature-like physiology in fast-spiking interneurons. These findings reveal a developmental window in which thalamic input shapes prefrontal inhibitory maturation, suggesting that some forms of cortical dysfunction in psychiatric disease originate not in the cortex itself, but in its thalamic inputs.
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