ORCID Profile
0000-0001-5153-5652
Current Organisation
University of Queensland
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Zoology | Animal Neurobiology | Evolution of Developmental Systems | Central Nervous System | Animal Cell and Molecular Biology | Animal Developmental and Reproductive Biology | Gene and Molecular Therapy | Neurosciences
Expanding Knowledge in the Biological Sciences | Nervous System and Disorders |
Publisher: Elsevier BV
Date: 10-2021
DOI: 10.1016/J.SEMCDB.2021.04.009
Abstract: The anterior commissure is the most ancient of the forebrain interhemispheric connections among all vertebrates. Indeed, it is the predominant pallial commissure in all non-eutherian vertebrates, universally subserving basic functions related to olfaction and survival. A key feature of the anterior commissure is its ability to convey connections from erse brain areas, such as most of the neocortex in non-eutherian mammals, thereby mediating the bilateral integration of erse functions. Shared developmental mechanisms between the anterior commissure and more evolutionarily recent commissures, such as the corpus callosum in eutherians, have led to the hypothesis that the former may have been a precursor for additional expansion of commissural circuits. However, differences between the formation of the anterior commissure and other telencephalic commissures suggest that independent developmental mechanisms underlie the emergence of these connections in extant species. Here, we review the developmental mechanisms and connectivity of the anterior commissure across evolutionarily distant species, and highlight its potential functional importance in humans, both in the course of normal neurodevelopment, and as a site of plastic axonal rerouting in the absence or damage of other connections.
Publisher: Springer Science and Business Media LLC
Date: 30-05-2017
Publisher: American Association for the Advancement of Science (AAAS)
Date: 09-04-2021
Abstract: In primates, visual connections are bilateral: Each eye sends neural connections to both sides of the brain. Vigouroux et al. looked at the evolutionary underpinnings of the bilateral visual system. A close look at the connections between the retina and the brain in a variety of fish species representing a span of evolutionary ergence revealed that contralateral connections seem to be universal. The ipsilateral connections, which add to the contralateral connections to form a bilateral visual system, arrived later in evolution but before the transition to land-dwelling animals. Science , this issue p. 150
Publisher: eLife Sciences Publications, Ltd
Date: 06-04-2018
DOI: 10.7554/ELIFE.61769
Abstract: The forebrain hemispheres are predominantly separated during embryogenesis by the interhemispheric fissure (IHF). Radial astroglia remodel the IHF to form a continuous substrate between the hemispheres for midline crossing of the corpus callosum (CC) and hippoc al commissure (HC). DCC and NTN1 are molecules that have an evolutionarily conserved function in commissural axon guidance. The CC and HC are absent in Dcc and Ntn1 knockout mice, while other commissures are only partially affected, suggesting an additional aetiology in forebrain commissure formation. Here, we find that these molecules play a critical role in regulating astroglial development and IHF remodelling during CC and HC formation. Human subjects with DCC mutations display disrupted IHF remodelling associated with CC and HC malformations. Thus, axon guidance molecules such as DCC and NTN1 first regulate the formation of a midline substrate for dorsal commissures prior to their role in regulating axonal growth and guidance across it.
Publisher: Proceedings of the National Academy of Sciences
Date: 22-05-2023
Abstract: The development of precise neural circuits in the brain requires spontaneous patterns of neural activity prior to functional maturation. In the rodent cerebral cortex, patchwork and wave patterns of activity develop in somatosensory and visual regions, respectively, and are present at birth. However, whether such activity patterns occur in noneutherian mammals, as well as when and how they arise during development, remain open questions relevant for understanding brain formation in health and disease. Since the onset of patterned cortical activity is challenging to study prenatally in eutherians, here we offer an approach in a minimally invasive manner using marsupial dunnarts, whose cortex forms postnatally. We discovered similar patchwork and travelling waves in the dunnart somatosensory and visual cortices at stage 27 (equivalent to newborn mice) and examined earlier stages of development to determine the onset of these patterns and how they first emerge. We observed that these patterns of activity emerge in a region-specific and sequential manner, becoming evident as early as stage 24 in somatosensory and stage 25 in visual cortices (equivalent to embryonic day 16 and 17, respectively, in mice), as cortical layers establish and thalamic axons innervate the cortex. In addition to sculpting synaptic connections of existing circuits, evolutionarily conserved patterns of neural activity could therefore help regulate other early events in cortical development.
Publisher: The Company of Biologists
Date: 02-2022
DOI: 10.1242/DEV.200212
Abstract: Only mammals evolved a neocortex, which integrates sensory-motor and cognitive functions. Significant ersifications in the cellular composition and connectivity of the neocortex occurred between the two main therian groups: marsupials and eutherians. However, the developmental mechanisms underlying these ersifications are largely unknown. Here, we compared the neocortical transcriptomes of Sminthopsis crassicaudata, a mouse-sized marsupial, with those of eutherian mice at two developmentally equivalent time points corresponding to deeper and upper layer neuron generation. Enrichment analyses revealed more mature gene networks in marsupials at the early stage, which reverted at the later stage, suggesting a more precocious but protracted neuronal maturation program relative to birth timing of cortical layers. We ranked genes expressed in different species and identified important differences in gene expression rankings between species. For ex le, genes known to be enriched in upper-layer cortical projection neuron subtypes, such as Cux1, Lhx2 and Satb2, likely relate to corpus callosum emergence in eutherians. These results show molecular heterochronies of neocortical development in Theria, and highlight changes in gene expression and cell type composition that may underlie neocortical evolution and ersification. This article has an associated 'The people behind the papers' interview.
Publisher: Proceedings of the National Academy of Sciences
Date: 04-09-2018
Abstract: The neocortex is a hallmark of mammalian evolution, and connections between both hemispheres integrate bilateral functions. In eutherians (e.g., rodents and humans), interhemispheric circuits course via the corpus callosum and share a similar connectome throughout species. Noneutherian mammals (i.e., monotremes and marsupials), however, did not evolve a corpus callosum therefore, whether the eutherian connectome arose as consequence of callosal evolution or instead reflects ancient connectivity principles remains unknown. We studied monotreme and marsupial interhemispheric neocortical connectomes and compared these with eutherian datasets. This revealed interhemispheric connectivity features shared across mammals, with or without a corpus callosum, suggesting that an ancient connectome originated at least 80 million years before callosal evolution.
Publisher: Elsevier BV
Date: 12-2018
DOI: 10.1016/J.CONB.2018.05.005
Abstract: Long-range projection neurons of the neocortex form the major tracts of the mammalian brain and are crucial for sensory-motor, associative and executive functions. Development of such circuits involves neuronal proliferation, specification and migration, as well as axonal elongation, navigation and targeting, where growing axons encounter multiple guidance cues and integrate these signals to execute guidance decisions. The complexity of axon guidance mechanisms in the formation of long-range neuronal projections has suggested that they might be under control of transcription factors, which are DNA-binding proteins that regulate the expression of downstream genes. Here we discuss recent advances in our understanding of the control of axon guidance by transcriptional regulation, as well as future directions for the elucidation of the mechanisms and pathological relevance of this process.
Publisher: Frontiers Media SA
Date: 14-07-2014
Publisher: Public Library of Science (PLoS)
Date: 07-09-2017
Publisher: SAGE Publications
Date: 2017
Abstract: Alterations in the development of neuronal connectivity can result in dramatic outcomes for brain function. In the cerebral cortex, most sensorimotor and higher-order functions require coordination between precise regions of both hemispheres through the axons that form the corpus callosum. However, little is known about how callosal axons locate and innervate their contralateral targets. Here, we use a combination of in utero electroporation, retrograde tracing, sensory deprivation and high-resolution axonal quantification to investigate the development, organisation and activity dependence of callosal axons arising from the primary somatosensory cortex of mice. We show that distinct contralateral projections arise from different neuronal populations and form homotopic and heterotopic circuits. Callosal axons innervate the contralateral hemisphere following a dorsomedial to ventrolateral and region-specific order. Furthermore, we identify two periods of region- and layer-specific developmental exuberance that correspond to initial callosal axon innervation and subsequent arborisation. Early sensory deprivation affects only the latter of these events. Taken together, these results reveal the main developmental events of contralateral callosal targeting and may aid future understanding of the formation and pathologies of brain connectivity.
Publisher: eLife Sciences Publications, Ltd
Date: 12-03-2021
Publisher: eLife Sciences Publications, Ltd
Date: 02-04-2021
Publisher: eLife Sciences Publications, Ltd
Date: 04-05-2021
DOI: 10.7554/ELIFE.61618
Abstract: Corpus callosum dysgenesis (CCD) is a congenital disorder that incorporates either partial or complete absence of the largest cerebral commissure. Remodelling of the interhemispheric fissure (IHF) provides a substrate for callosal axons to cross between hemispheres, and its failure is the main cause of complete CCD. However, it is unclear whether defects in this process could give rise to the heterogeneity of expressivity and phenotypes seen in human cases of CCD. We identify incomplete IHF remodelling as the key structural correlate for the range of callosal abnormalities in inbred and outcrossed BTBR mouse strains, as well as in humans with partial CCD. We identify an eight base-pair deletion in Draxin and misregulated astroglial and leptomeningeal proliferation as genetic and cellular factors for variable IHF remodelling and CCD in BTBR strains. These findings support a model where genetic events determine corpus callosum structure by influencing leptomeningeal-astroglial interactions at the IHF.
Publisher: Proceedings of the National Academy of Sciences
Date: 20-04-2020
Abstract: The corpus callosum connects left and right cerebral cortices, integrating sensory-motor and associative functions, and is the largest connection in the human brain. While all mammals have a cerebral cortex, only eutherians evolved a corpus callosum. However, how this occurred remains largely unknown. We compared transcription factors that control subcerebral versus callosal neuron projection fates in eutherians and marsupials and found remarkably high similarity of their gene sequences and functions. However, expression of the callosal gene SATB2 was delayed in mice relative to dunnarts, and premature overexpression was sufficient for reversion to an ancestral-like brain phenotype. Our results suggest that transcriptional heterochrony might have influenced callosal evolution, and that complex traits can originate by differential deployment of existing regulatory genes.
Publisher: Elsevier BV
Date: 2018
DOI: 10.1016/J.JNEUMETH.2017.09.004
Abstract: The technique of in utero electroporation has been widely used in eutherians, such as mice and rats, to investigate brain development by selectively manipulating gene expression in specific neuronal populations. A major challenge, however, is that surgery is required to access the embryos, affecting animal survival and limiting the number of times it can be performed within the same litter. Marsupials are born at an early stage of brain development as compared to eutherians. Forebrain neurogenesis occurs mostly postnatally, allowing electroporation to be performed while joeys develop attached to the teat. Here we describe the method of in pouch electroporation using the Australian marsupial fat-tailed dunnart (Sminthopsis crassicaudata, Dasyuridae). In pouch electroporation is minimally invasive, quick, successful and anatomically precise. Moreover, as no surgery is required, it can be performed several times in the same in idual, and littermates can undergo independent treatments. As compared to in utero electroporation in rodents, in pouch electroporation in marsupials offers unprecedented opportunities to study brain development in a minimally invasive manner. Continuous access to developing joeys during a protracted period of cortical development allows multiple and independent genetic manipulations to study the interaction of different systems during brain development. In pouch electroporation in marsupials offers an excellent in vivo assay to study forebrain development and evolution. By combining developmental, functional and comparative approaches, this system offers new avenues to investigate questions of biological and medical relevance, such as the precise mechanisms of brain wiring and the organismic and environmental influences on neural circuit formation.
Publisher: Cold Spring Harbor Laboratory
Date: 19-02-2023
DOI: 10.1101/2023.02.18.529078
Abstract: The development of precise neural circuits in the brain requires spontaneous patterns of neural activity prior to functional maturation. In the rodent cerebral cortex patchwork and wave patterns of activity develop in somatosensory and visual regions, respectively, and are present at birth. However, whether such activity patterns occur in non-eutherian mammals, as well as when and how they arise during development remain open questions relevant to understand brain formation in health and disease. Since the onset of patterned cortical activity is challenging to study prenatally in eutherians, here we offer a new approach in a minimally invasive manner using marsupial dunnarts, whose cortex forms postnatally. We discovered similar patchwork and travelling waves in the dunnart somatosensory and visual cortices at stage 27 (equivalent to newborn mice), and examined progressively earlier stages of development to determine their onset and how they first emerge. We observed that these patterns of activity emerge in a region-specific and sequential manner, becoming evident as early as stage 24 in somatosensory and stage 25 in visual cortices (equivalent to embryonic day 16 and 17, respectively, in mice), as cortical layers establish and thalamic axons innervate the cortex. In addition to sculpting synaptic connections of existing circuits, evolutionarily conserved patterns of neural activity could therefore help regulate early events in cortical development. Region-specific patterns of neural activity are present at birth in rodents and are thought to refine synaptic connections during critical periods of cerebral cortex development. Marsupials are born much more immature than rodents, allowing the investigation of how these patterns arise in vivo. We discovered that cortical activity patterns are remarkably similar in marsupial dunnarts and rodents, and that they emerge very early, before cortical neurogenesis is complete. Moreover, they arise from the outset in different patterns specific to somatosensory and visual areas (i.e., patchworks and waves) indicating they may also play evolutionarily conserved roles in cortical regionalization during development.
Publisher: Proceedings of the National Academy of Sciences
Date: 31-07-2023
Abstract: The thylacine, or Tasmanian tiger, is the largest of modern-day carnivorous marsupials and was hunted to extinction by European settlers in Australia. Its physical resemblance to eutherian wolves is a striking ex le of evolutionary convergence to similar ecological niches. However, whether the neuroanatomical organization of the thylacine brain resembles that of canids and how it compares with other mammals remain unknown due to the scarcity of available s les. Here, we gained access to a century-old hematoxylin-stained histological series of a thylacine brain, digitalized it at high resolution, and compared its forebrain cellular architecture with 34 extant species of monotremes, marsupials, and eutherians. Phylogenetically informed comparisons of cortical folding, regional volumes, and cell sizes and densities across cortical areas and layers provide evidence against brain convergences with canids, instead demonstrating features typical of marsupials, and more specifically Dasyuridae, along with traits that scale similarly with brain size across mammals. Enlarged olfactory, limbic, and neocortical areas suggest a small-prey predator and/or scavenging lifestyle, similar to extant quolls and Tasmanian devils. These findings are consistent with a nonuniformity of trait convergences, with brain traits clustering more with phylogeny and head/body traits with lifestyle. By making this resource publicly available as rapid web-accessible, hierarchically organized, multiresolution images for perpetuity, we anticipate that additional comparative insights might arise from detailed studies of the thylacine brain and encourage researchers and curators to share, annotate, and preserve understudied material of outstanding biological relevance.
Start Date: 2020
End Date: 12-2023
Amount: $449,250.00
Funder: Australian Research Council
View Funded ActivityStart Date: 2016
End Date: 12-2018
Amount: $372,000.00
Funder: Australian Research Council
View Funded ActivityStart Date: 2016
End Date: 12-2019
Amount: $592,700.00
Funder: Australian Research Council
View Funded Activity