Neuroanatomical mapping of gerbil corticostriatal and thalamostriatal projections reveals the parafascicular nucleus as a relay for vestibular information to the entire striatum.
Jared B Smith, Sean S Hong, Damian J Murphy, Evelynne Dangcil, Jacqueline Nacipucha, Aaron Tucker, Nicolas L Carayannopoulos, Mina Beshy, Shrivaishnavi Chandrasekar, Eran Peci, Matthew Y Kiel, P Ashley Wackym, Justin D Yao, Todd M Mowery
{"title":"Neuroanatomical mapping of gerbil corticostriatal and thalamostriatal projections reveals the parafascicular nucleus as a relay for vestibular information to the entire striatum.","authors":"Jared B Smith, Sean S Hong, Damian J Murphy, Evelynne Dangcil, Jacqueline Nacipucha, Aaron Tucker, Nicolas L Carayannopoulos, Mina Beshy, Shrivaishnavi Chandrasekar, Eran Peci, Matthew Y Kiel, P Ashley Wackym, Justin D Yao, Todd M Mowery","doi":"10.1523/ENEURO.0246-24.2025","DOIUrl":null,"url":null,"abstract":"<p><p>The striatum is the primary input nucleus of the basal ganglia, integrating a dense plexus of inputs from the cerebral cortex and thalamus to regulate action selection and learning. Neuroanatomical mapping of the striatum and its sub compartments has been carried out extensively in rats and mice, non-human primates, and cats allowing comparative neuroanatomy studies to derive heuristics about striatal composition and function. Here, we systematically map corticostriatal topography from motor, somatosensory, auditory, and visual cortices as well as thalamostriatal parafascicular (PfN) inputs in the Mongolian Gerbil. We also map a pathway reported in mice from medial vestibular nucleus to the PfN that could convey vestibular information to the striatum. Our findings align with those of similar studies in other rodents, indicating homologous neuroanatomical connectivity patterns within the corticostriatal projectome across rodentia. We observed corticostriatal peaks of dense labeling for each input with a diffuse projection throughout striatal subregions from each cortical region, suggesting a global integration of all cortical information by the striatum. Thalamostriatal projections from PfN covered most of the striatum with a peak of PfN specific compartmentalized labeling similar to other sensory and motor systems. We also confirm the connection from the medial vestibular nucleus to PfN thalamus, indicating that vestibular information may be widely integrated throughout the striatum. The findings build upon our body of knowledge on striatal connectivity across mammalian species and provide a foundation for striatal research focusing on vestibulothalamostriatal circuits in rodentia.<b>Significance statement</b> In this study, systematic mapping of the projections to striatum from motor, somatosensory, auditory, and visual cortices in Mongolian gerbil reveal commonalities with rodents. Principally, while some areas receive compartmentalized innervation from specific modalities, there also exists a global interspersed plexus of integrating inputs from each cortical area to each striatal subregion. Additionally, we also demonstrate a clear thalamostriatal innervation from parafascicular thalamus (PfN), that is homologous to other rodents and primates. Finally, we confirm a pathway from the medial vestibular nucleus to PfN thalamus that could broadly convey vestibular information across the striatum. Our results reveal common principles in neuroanatomical connectivity across another mammalian species and provide an anatomical map to guide future vestibular striatal studies in gerbils and other animal models.</p>","PeriodicalId":11617,"journal":{"name":"eNeuro","volume":" ","pages":""},"PeriodicalIF":2.7000,"publicationDate":"2025-02-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"eNeuro","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1523/ENEURO.0246-24.2025","RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q3","JCRName":"NEUROSCIENCES","Score":null,"Total":0}
引用次数: 0
Abstract
The striatum is the primary input nucleus of the basal ganglia, integrating a dense plexus of inputs from the cerebral cortex and thalamus to regulate action selection and learning. Neuroanatomical mapping of the striatum and its sub compartments has been carried out extensively in rats and mice, non-human primates, and cats allowing comparative neuroanatomy studies to derive heuristics about striatal composition and function. Here, we systematically map corticostriatal topography from motor, somatosensory, auditory, and visual cortices as well as thalamostriatal parafascicular (PfN) inputs in the Mongolian Gerbil. We also map a pathway reported in mice from medial vestibular nucleus to the PfN that could convey vestibular information to the striatum. Our findings align with those of similar studies in other rodents, indicating homologous neuroanatomical connectivity patterns within the corticostriatal projectome across rodentia. We observed corticostriatal peaks of dense labeling for each input with a diffuse projection throughout striatal subregions from each cortical region, suggesting a global integration of all cortical information by the striatum. Thalamostriatal projections from PfN covered most of the striatum with a peak of PfN specific compartmentalized labeling similar to other sensory and motor systems. We also confirm the connection from the medial vestibular nucleus to PfN thalamus, indicating that vestibular information may be widely integrated throughout the striatum. The findings build upon our body of knowledge on striatal connectivity across mammalian species and provide a foundation for striatal research focusing on vestibulothalamostriatal circuits in rodentia.Significance statement In this study, systematic mapping of the projections to striatum from motor, somatosensory, auditory, and visual cortices in Mongolian gerbil reveal commonalities with rodents. Principally, while some areas receive compartmentalized innervation from specific modalities, there also exists a global interspersed plexus of integrating inputs from each cortical area to each striatal subregion. Additionally, we also demonstrate a clear thalamostriatal innervation from parafascicular thalamus (PfN), that is homologous to other rodents and primates. Finally, we confirm a pathway from the medial vestibular nucleus to PfN thalamus that could broadly convey vestibular information across the striatum. Our results reveal common principles in neuroanatomical connectivity across another mammalian species and provide an anatomical map to guide future vestibular striatal studies in gerbils and other animal models.
期刊介绍:
An open-access journal from the Society for Neuroscience, eNeuro publishes high-quality, broad-based, peer-reviewed research focused solely on the field of neuroscience. eNeuro embodies an emerging scientific vision that offers a new experience for authors and readers, all in support of the Society’s mission to advance understanding of the brain and nervous system.