Region-selective control of the thalamic reticular nucleus via cortical layer 5 pyramidal cells

Hádinger, Nóra; Bősz, Emília; Tóth, Boglárka; Vantomme, Gil; Lüthi, Anita; Acsády, László

doi:10.1038/s41593-022-01217-z

Cited by 16 publications

(7 citation statements)

References 57 publications

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“…GABAergic axons from the basal ganglia output nuclei (SNr and ENT) are prominent sources of input to the ventral motor thalamus. In addition, as all other nuclei of the thalamus, the motor nuclei receive GABAergic input from the reticular prethalamic nucleus ( Hádinger et al, 2023 ). To gain insight on the spatial distribution of these important inputs in the ventral motor nuclei neuropil we immunostained for two specific markers of presynaptic vesicle pools in GABAergic axon terminals, the vesicular GABA transporter (vGAT) and the enzyme glutamate decarboxylase 65/67 (GAD65/67; Esclapez et al, 1994 ).…”

Section: Resultsmentioning

confidence: 99%

Cerebellar and basal ganglia inputs define three main nuclei in the mouse ventral motor thalamus

Alonso-Martínez,

Rubio-Teves,

Casas-Torremocha

et al. 2023

Front. Neuroanat.

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The thalamus is a central link between cortical and subcortical brain motor systems. Axons from the deep nuclei of the cerebellum (DCN), or the output nuclei of the basal ganglia system (substantia nigra reticulata, SNr; and internal pallidum GPi/ENT) monosynaptically innervate the thalamus, prominently some nuclei of the ventral nuclear group. In turn, axons from these ventral nuclei innervate the motor and premotor areas of the cortex, where their input is critical for planning, execution and learning of rapid and precise movements. Mice have in recent years become a widely used model in motor system research. However, information on the distribution of cerebellar and basal ganglia inputs in the rodent thalamus remains poorly defined. Here, we mapped the distribution of inputs from DCN, SNr, and GPi/ENT to the ventral nuclei of the mouse thalamus. Immunolabeling for glutamatergic and GABAergic neurotransmission markers delineated two distinct main territories, characterized each by the presence of large vesicular glutamate transporter type 2 (vGLUT2) puncta or vesicular GABA transporter (vGAT) puncta. Anterograde labeling of axons from DCN revealed that they reach virtually all parts of the ventral nuclei, albeit its axonal varicosities (putative boutons) in the vGAT-rich sector are consistently smaller than those in the vGLUT2-rich sector. In contrast, the SNr axons innervate the whole vGAT-rich sector, but not the vGLUT2-rich sector. The GPi/ENT axons were found to innervate only a small zone of the vGAT-rich sector which is also targeted by the other two input systems. Because inputs fundamentally define thalamic cell functioning, we propose a new delineation of the mouse ventral motor nuclei that is consistent with the distribution of DCN, SNr and GPi/ENT inputs and resembles the general layout of the ventral motor nuclei in primates.

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Section: Resultsmentioning

confidence: 99%

Cerebellar and basal ganglia inputs define three main nuclei in the mouse ventral motor thalamus

Alonso-Martínez,

Rubio-Teves,

Casas-Torremocha

et al. 2023

Front. Neuroanat.

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“…Intriguingly, despite the caudal location of Pf within the thalamus, the TRN neurons that innervate it are located in a rostral and ventral part of TRN. The same TRN zone has been reported to project back to Pf in rats ( Kolmac and Mitrofanis, 1997 ) and to be selectively targeted by the axons from other motor thalamic nuclei, as well as by corticothalamic axons from the motor cortex ( Hádinger et al, 2023 ).…”

Section: Discussionmentioning

confidence: 75%

Micropopulation mapping of the mouse parafascicular nucleus connections reveals diverse input–output motifs

Gonzalo-Martín,

Alonso-Martínez,

Sepúlveda

et al. 2024

Front. Neuroanat.

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IntroductionIn primates, including humans, the centromedian/parafascicular (CM-Pf) complex is a key thalamic node of the basal ganglia system. Deep brain stimulation in CM-Pf has been applied for the treatment of motor disorders such as Parkinson’s disease or Tourette syndrome. Rodents have become widely used models for the study of the cellular and genetic mechanisms of these and other motor disorders. However, the equivalence between the primate CM-Pf and the nucleus regarded as analogous in rodents (Parafascicular, Pf) remains unclear.MethodsHere, we analyzed the neurochemical architecture and carried out a brain-wide mapping of the input–output motifs in the mouse Pf at micropopulation level using anterograde and retrograde labeling methods. Specifically, we mapped and quantified the sources of cortical and subcortical input to different Pf subregions, and mapped and compared the distribution and terminal structure of their axons.ResultsWe found that projections to Pf arise predominantly (>75%) from the cerebral cortex, with an unusually strong (>45%) Layer 5b component, which is, in part, contralateral. The intermediate layers of the superior colliculus are the main subcortical input source to Pf. On its output side, Pf neuron axons predominantly innervate the striatum. In a sparser fashion, they innervate other basal ganglia nuclei, including the subthalamic nucleus (STN), and the cerebral cortex. Differences are evident between the lateral and medial portions of Pf, both in chemoarchitecture and in connectivity. Lateral Pf axons innervate territories of the striatum, STN and cortex involved in the sensorimotor control of different parts of the contralateral hemibody. In contrast, the mediodorsal portion of Pf innervates oculomotor-limbic territories in the above three structures.DiscussionOur data thus indicate that the mouse Pf consists of several neurochemically and connectively distinct domains whose global organization bears a marked similarity to that described in the primate CM-Pf complex.

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“…There are no recurrent connections in the thalamus within or across thalamic nuclei ( Jones, 2007 ). The effect of thalamic reticular nucleus neurons was included indirectly as a constant inhibitory current to all thalamic areas ( Crabtree, 2018 ; Hádinger et al, 2023 ). Similarly to cortical areas, the thalamus is organized along a measured hierarchy ( Harris et al, 2019 ).…”

Section: Resultsmentioning

confidence: 99%

Cell type-specific connectome predicts distributed working memory activity in the mouse brain

Ding,

Froudist-Walsh,

Jaramillo

et al. 2024

eLife

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Recent advances in connectome and neurophysiology make it possible to probe whole-brain mechanisms of cognition and behavior. We developed a large-scale model of the mouse multiregional brain for a cardinal cognitive function called working memory, the brain's ability to internally hold and process information without sensory input. The model is built on mesoscopic connectome data for inter-areal cortical connections and endowed with a macroscopic gradient of measured parvalbumin-expressing interneuron density. We found that working memory coding is distributed yet exhibits modularity; the spatial pattern of mnemonic representation is determined by long-range cell type-specific targeting and density of cell classes. Cell type-specific graph measures predict the activity patterns and a core subnetwork for memory maintenance. The model shows numerous self-sustained internal states (each engaging a distinct subset of areas). This work provides a framework to interpret large-scale recordings of brain activity during cognition, while highlighting the need for cell type-specific connectomics.

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Region-selective control of the thalamic reticular nucleus via cortical layer 5 pyramidal cells

Cited by 16 publications

References 57 publications

Cerebellar and basal ganglia inputs define three main nuclei in the mouse ventral motor thalamus

Cerebellar and basal ganglia inputs define three main nuclei in the mouse ventral motor thalamus

Micropopulation mapping of the mouse parafascicular nucleus connections reveals diverse input–output motifs

Cell type-specific connectome predicts distributed working memory activity in the mouse brain

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