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Bourne, J. A.

Publications and source records attributed to Bourne, J. A..

9 recordsLinked to original sources

Robust and accessible in situ sequencing with an open-source automated sequencer

Targeted in situ sequencing underlies many spatial transcriptomic, barcoded connectomic, and multiplexed perturbation techniques. Each experiment requires many cycles of chemical reactions and imaging that are time-consuming and error-prone to perform manually, and few commercial platforms can sequence highly diverse RNA barcodes in situ at cellular resolution across large tissue sections. Here we present Seq-o-Matic, an open-source automated in situ sequencer built entirely from commercially available components, which integrates fluidics, heated incubation, and imaging of up to three continuous 18 mm x 50 mm areas on standard microscope slides. Relative to manual sequencing, Seq-o-Matic reduced hands-on time 6- to 17.5-fold and total run time about 2.6-fold. Across three runs spanning two mouse strains and a neonatal marmoset, sequencing quality, measured by signal retention, channel specificity, and phasing, was similar to that of four manually sequenced mouse brains. In four mouse hemispheres sequenced in separate runs (two C57BL/6J, one NOD, and one WSB), consensus cell types were present in every brain and corresponded to those of a manually sequenced C57BL/6J brain. Within cortical excitatory neurons, the two C57BL/6J brains were more similar to each other than were brains of different strains, suggesting that technical variation between runs was small relative to strain differences. Seq-o-Matic thus makes consistent, high-throughput in situ sequencing accessible to laboratories without specialized in situ sequencing expertise.

genomics↗

Early-life medial pulvinar disruption drives schizophrenia-relevant prefrontal inhibitory and cognitive deficits in primates

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.

neuroscience↗

Conserved and specialized features of thalamocortical wiring revealed by single-cell projection mapping in mouse and marmoset

Across mammals, brain regions can duplicate, expand, and diversify, requiring long-range connectivity to accommodate species-specific specializations while preserving globally ordered wiring. This challenge is especially pronounced in primate thalamocortical circuits, where select cortical fields and their thalamic partners have expanded disproportionately. Although gene expression in the thalamus follows broad and conserved gradients, how thalamocortical projections are organized at single-neuron resolution, and how this organization is reshaped by expansion, remain unknown. Here, we investigate thalamocortical projection organization by in situ sequencing and BARseq projection mapping in marmosets and mice. We profiled the gene expression of 1.5 million marmoset neurons and jointly measured gene expression and cortical projections in 708 marmoset and 1,518 mouse neurons that spanned multiple thalamic nuclei. In both species, projections of individual neurons targeted diverse areas that together spanned a large fraction of the cortex. Comparing projections at the single-neuron level and local neighborhood level revealed that marmoset thalamocortical projections were more spatially segregated, producing a point-to-point architecture. Strikingly, this local specialization coexisted with a conserved gradient that predominated over discrete anatomical borders: In the higher-order sensory thalamus of both species, gene expression and projections varied continuously across nucleus borders, and borders had only a small effect on projections. Furthermore, in both marmoset and mouse, gene expression gradients were associated with the anteroposterior locations of cortical targets. These results reconcile discrete nucleus and gradient-based models of thalamic organization and suggest that primate circuit specialization is superimposed on a conserved molecular-projection gradient.

neuroscience↗

Widespread Corticothalamic Connectivity Identifies the Inferior Pulvinar as a Central Node in Visual Network Architecture

The medial subdivision of the inferior pulvinar (PIm) has been implicated in motion processing, visuomotor integration, and residual visual function, yet a comprehensive account of its cortical inputs remains unresolved. Previous studies often relied on indirect cortical injections or tracer deposits spanning multiple pulvinar subdivisions, limiting anatomical specificity. Here, we used MRI-guided, cytoarchitectonically restricted retrograde tracer injections to selectively target PI in the common marmoset (Callithrix jacchus) and systematically map its cortical afferents. Across four cases, retrogradely labeled neurons were widely distributed throughout occipital, temporal, parietal, and cingulate cortices, with a strong predominance in layer V, consistent with driver-like corticothalamic projections. Early and middle-tier visual areas (V1, V2, V3, V3A, V4, V6/DM) contributed substantial input, with labeling patterns corresponding to peripheral visual field representations. The middle temporal complex (MT, MTc, MST, FST) represented one of the densest sources of cortical projections. Prominent inputs also arose from posterior parietal regions, including LIP, MIP, VIP, AIP, and inferior parietal areas (e.g., PFG, OPt), linking PIm to visuospatial and action-related networks. Semi-quantitative analyses indicated that occipital cortex and the MT complex together accounted for approximately 60% of total cortical input, while parietal cortex contributed roughly 20%. Additional projections from retrosplenial and posterior cingulate cortices were observed. These findings identify PIm as a central integrative node embedded within distributed visual and visuomotor networks. Rather than functioning as a restricted visual relay, PIm appears positioned to coordinate motion, spatial, and action-relevant signals within cortico-thalamocortical circuits supporting adaptive visually-guided behavior.

neuroscience↗

Developmental dynamics of the prefrontal cortical SST and PV interneuron networks: Insights from the monkey highlight human-specific features

The primate prefrontal cortex (PFC) is a quintessential hub of cognitive functions. Amidst its intricate neural architecture, the interplay of distinct neuronal subtypes, notably parvalbumin (PV) and somatostatin (SST) interneurons (INs), emerge as a cornerstone in sculpting cortical circuitry and governing cognitive processes. While considerable strides have been made in elucidating the developmental trajectory of these neurons in rodent models, our understanding of their postmigration developmental dynamics in primates still needs to be studied. Disruptions to this developmental trajectory can compromise IN function, impairing signal gating and circuit modulation within cortical networks. This study examined the expression patterns of PV and SST, ion transporter KCC2, and ion channel subtypes Kv3.1b, and Nav1.1 -associated with morphophysiological stages of development in the postnatal marmoset monkey in different frontal cortical regions (granular areas 8aD, 8aV, 9, 46; agranular areas 11, 47L). Our results demonstrate that the maturation of PV+ INs extends into adolescence, characterized by discrete epochs associated with specific expression dynamics of ion channel subtypes. Interestingly, we observed a postnatal decrease in SST interneurons, contrasting with studies in rodents. This endeavor broadens our comprehension of primate cortical development and furnishes invaluable insights into the etiology and pathophysiology of neurodevelopmental disorders characterized by perturbations in PV and SST IN function. Summary StatementThe prefrontal cortex (PFC) in primates is crucial for cognitive functions, with parvalbumin (PV) and somatostatin (SST) interneurons playing key roles. This study in marmoset monkeys explores their developmental dynamics, revealing prolonged maturation of PV interneurons and contrasting SST patterns from rodents, enhancing understanding of primate cortical development.

neuroscience↗

Dynamic fibroblast-immune interactions shape wound healing after brain injury

Fibroblasts coordinate the response to tissue injury, directing organ regeneration versus scarring. In the central nervous system (CNS), fibroblasts are uncommon cells enriched at tissue borders, and their molecular, cellular, and functional interactions after brain injury are poorly understood. Here we define the fibroblast response to sterile brain damage across time and space. Early pro-fibrotic myofibroblasts infiltrated CNS lesions and were functionally and spatially organized by fibroblast TGF{beta} signaling, pro-fibrotic macrophages and microglia, and perilesional brain glia that activated TGF{beta} via integrin v{beta}8. Early myofibroblasts subsequently transitioned into a variety of late states, including meningeal and lymphocyte-interactive fibroblasts that persisted long term. Interruption of this dynamic fibroblast-macrophage-glial coordination impaired brain wound healing and the resolution of neuroinflammation, disrupted generation of late de novo CNS lymphocyte niches, and increased mortality in a stroke model. This work highlights an unexpected role of fibroblasts as coordinate regulators of CNS healing and neuroinflammation after brain injury.

immunology↗

Replicating infant astrocyte behavior in the adult after brain injury improves outcomes

Infants and adults respond differently to brain injuries. Specifically, improved neuronal sparing along with reduced astrogliosis and glial scarring often observed earlier in life, likely contributes to improved long-term outcomes. Understanding the underlying mechanisms could enable the recapitulation of neuroprotective effects, observed in infants, to benefit adult patients after brain injuries. We reveal that in primates, Eph/ ephrin signaling contributes to age-dependent reactive astrocyte behavior. Ephrin-A5 expression on astrocytes was more protracted in adults, whereas ephrin-A1 was associated only with infant astrocytes. Furthermore, ephrin-A5 exacerbated major hallmarks of astrocyte reactivity via EphA2 and EphA4 receptors, which was subsequently alleviated by ephrin-A1. Rather than suppressing reactivity, ephrin-A1 signaling shifted astrocytes towards GAP43+ neuroprotection, accounting for improved neuronal sparing in infants. Reintroducing ephrin-A1 after middle-aged ischemic stroke significantly attenuated glial scarring, improved neuronal sparing and preserved circuitry. Therefore, beneficial infant mechanisms can be recapitulated in adults to improve outcomes after CNS injuries.

neuroscience↗

Primate-specific response of astrocytes to stroke limits peripheral macrophage infiltration

Reactive astrocytes play critical roles after brain injuries but their precise function in stroke is not well defined. Here, we utilized single nuclei transcriptomics to characterize astrocytes after ischemic stroke in nonhuman primate (NHP) marmoset monkey primary visual cortex. We identified 19 putative subtypes of astrocytes from injured and uninjured brain hemispheres and observed nearly complete segregation between stroke and control astrocyte clusters. We then screened for genes that might be limiting stroke recovery and discovered that one neurite-outgrowth inhibitory protein, NogoA, previously associated with oligodendrocytes but not astrocytes, was expressed in numerous reactive astrocyte subtypes. NogoA upregulation on reactive astrocytes was confirmed in vivo for NHP and human, but not observed to the same extent in rodent. Further in vivo and in vitro studies determined that NogoA mediated an anti-inflammatory response which limits deeper infiltration of peripheral macrophages from the lesion during the subacute post-stroke period. Specifically, these findings are relevant to the development of NogoA-targeting therapies shortly after ischemic stroke. Our findings have uncovered the complexity and species specificity of astrocyte responses, which need to be considered more when investigating novel therapeutics for brain injury.

neuroscience↗

Mapping the neural circuitry of predator fear in the nonhuman primate

In rodents, innate and learned fear of predators depends on the medial hypothalamic defensive system, a conserved brain network that lies downstream of the amygdala. However, it remains unknown whether this network is involved in primate fear. Here we demonstrate that visually evoked predator fear recruits a homologous medial hypothalamic defense system in the nonhuman primate

neuroscience↗