Proprioceptive thalamus receiving forelimb and neck muscle spindle inputs via the external cuneate nucleus in the rat

Uemura, Yume; Haque, Tahsinul; Satô, Fumihiko; Tsutsumi, Yumi; Ohara, Hisanori; Oka, Atsuhiro; Furuta, Takeshi; Bae, Yong Chul; Yamashiro, Takashi; Tachibana, Yoshihisa; Yoshida, Atsushi

doi:10.1007/s00429-020-02118-2

Cited by 20 publications

(14 citation statements)

References 48 publications

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“…These fibers convey low-threshold, mechanoreceptive primary afferents encoding pressure/distortion and target mainly the ventroposterior lateral nucleus (Graziano et al, 2008). We observed that, in addition, DCN axons target the dorsal and central region of the nucleus, in a pattern equivalent to that described in rat Po (Lund and Webster, 1967;Villanueva et al, 1998;Uemura et al, 2020). In addition, we show that DCN axons form the large immunopositive boutons that abound in the vGLUT2-rich dorsal domain of Po, a finding in register with the fact that the DCN projection neurons express intense vGLUT2 mRNA signal (Hisano et al, 2002).…”

Section: Dcn and Spinal Cord Inputssupporting

confidence: 61%

“…Po receives most of its ascending projections from neurons in the interpolaris spinal trigeminal nuclei (SpVI; Jacquin et al, 1989;Pierret et al, 2000;Veinante et al, 2000a) and thus have driver characthersitis (Lavallee et al, 2005). In addition, other subcortical structures such as dorsal column nuclei (DCN; Lund and Webster, 1967;Uemura et al, 2020) and the spinal cord (Iwata et al, 1992;Gauriau and Bernard, 2004) also project to Po, at least in rats.…”

Section: Introductionmentioning

confidence: 99%

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A combinatorial input landscape in the “higher-order relay” posterior thalamic nucleus

et al. 2022

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A large part of the thalamus is not directly involved in relaying ascending sensory inputs to the cerebral cortex. The functions and wiring of such "non-primary" nuclei remain unclear. The Posterior nucleus, a representative "non-primary" nucleus of the rodent thalamus, receives heavy and powerful inputs from cortical layer 5 (L5) cells. In addition, Po receives also some trigeminal, spinal and superior colliculus (SC) inputs, as well as powerful inhibitory inputs from the zona incerta (ZI) and anterior pretectal nucleus (APT). To elucidate to which extent these input systems converge or remain separate within Po, we first mapped the distribution of terminals immunolabeled for markers of glutamatergic or GABAergic neurotransmission and L5 terminals constitutively labeled in Rbp4-Cre;Ai14 mice. Besides, we retrogradely traced and quantified the sources of brain and spinal cord input reaching different Po regions. In addition, we compared bouton sizes in axons anterogradely labeled from the above input sources. Our data delineate several domains within Po, each dominated by specific sets of inputs. Cortical L5 afferents predominate in central and ventral Po. In contrast, large glutamatergic terminals from the trigeminal complex and spinal cord as well as GABAergic terminals from APT and ZI prevail in rostral and dorsal Po, and along the border with the ventral posteromedial nucleus. SC inputs preferentially target dorsal and caudal Po. These findings reveal multiple partly overlapping domains within Po. Hence, thalamic neuron subpopulations in different parts of Po may integrate diverse combinations of tactile, motor and pain-related inputs and give rise to functionally diverse thalamocortical subnetworks. Significance statementMany nuclei of the thalamus are not involved in relaying to cortex new information about the world or the body. The functions and wiring of such "non-primary" nuclei remain unclear. Here, we first mapped across the brain and spinal cord the origin of the input pathways reaching the Posterior nucleus, a typical non-primary relay nucleus.Then, we analyzed input distribution within the nucleus and, as a proxy for synaptic strength, the size of their axon terminals. We report a complex tridimensional mosaic of partly overlapping input-specific domains and significant bouton size differences. This wiring may allow diverse inputs to converge in graded combinatorial fashion onto thalamic cell subpopulations, hence giving rise to emergent computations and functionally diverse thalamocortical subnetworks.

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Section: Dcn and Spinal Cord Inputssupporting

confidence: 61%

Section: Introductionmentioning

confidence: 99%

A combinatorial input landscape in the “higher-order relay” posterior thalamic nucleus

et al. 2022

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“…the “non-conscious” pathway). In addition to the cerebellar projection, a thalamic projection from the ECu has been confirmed in primates 15 , raccoons 16 and rats 17 , but seems not be present in cats 18 . It has thus been suggested that this “conscious” pathway is phylogenetically recent and important for dexterous limb movements 13 .…”

Section: Resultsmentioning

confidence: 99%

Peripersonal encoding of forelimb proprioception in the mouse somatosensory cortex

Alonso

Palacio-Manzano

Scheer

et al. 2022

Preprint

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Conscious perception of limb movements depends on proprioceptive neural responses in the somatosensory cortex. In contrast to tactile sensations, proprioceptive cortical coding is barely studied in the mammalian brain and practically non-existent in rodent research. To understand the cortical representation of this important sensory modality we developed a passive forelimb displacement paradigm in behaving mice. We imaged the responses of layer 2/3 neurons with two-photon microscopy and tracked the 3D position of limb joints. In addition, mice were trained to perceptually discriminate proprioceptive stimuli allowing us to delineate the mouse proprioceptive cortex with optogenetic silencing experiments. Our results reveal that passive forelimb movements are preferentially encoded as a spatial direction vector that interfaces movements with behaviorally relevant targets. This neural representation of proprioception appears not to be limited to the somatosensory cortex.

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“…Mechanoreceptors in the skin, muscle, and joints receive information on touch, vibration and proprioception, and these receptors project via the dorsal column medial-lemniscal pathway to the dorsal column nuclei complex (DCN), which comprises the gracile and cuneate nuclei (Loutit et al, 2021 ). The DCN complex in turn has excitatory projections to the ventral posterior lateral and ventral posterior medial (i.e., somatosensory) nuclei of the thalamus (Kramer et al, 2017 ; Uemura et al, 2020 ), as well as projections to the zona incerta, red nucleus, cerebellar cortex, and IO (Boivie, 1971 ; Robinson et al, 1987 ; McCurdy et al, 1998 ; Quy et al, 2011 ). Therefore, the combination of somatosensory feedback of tremor and direct cerebellar-thalamic projections may contribute to the amplification or spread of tremor oscillations in the thalamus during movement.…”

Section: Discussionmentioning

confidence: 99%

Cerebello-Thalamo-Cortical Network Dynamics in the Harmaline Rodent Model of Essential Tremor

Woodward

Apps

Goodfellow

et al. 2022

Front. Syst. Neurosci.

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Essential Tremor (ET) is a common movement disorder, characterised by a posture or movement-related tremor of the upper limbs. Abnormalities within cerebellar circuits are thought to underlie the pathogenesis of ET, resulting in aberrant synchronous oscillatory activity within the thalamo-cortical network leading to tremors. Harmaline produces pathological oscillations within the cerebellum, and a tremor that phenotypically resembles ET. However, the neural network dynamics in cerebellar-thalamo-cortical circuits in harmaline-induced tremor remains unclear, including the way circuit interactions may be influenced by behavioural state. Here, we examined the effect of harmaline on cerebello-thalamo-cortical oscillations during rest and movement. EEG recordings from the sensorimotor cortex and local field potentials (LFP) from thalamic and medial cerebellar nuclei were simultaneously recorded in awake behaving rats, alongside measures of tremor using EMG and accelerometery. Analyses compared neural oscillations before and after systemic administration of harmaline (10 mg/kg, I.P), and coherence across periods when rats were resting vs. moving. During movement, harmaline increased the 9–15 Hz behavioural tremor amplitude and increased thalamic LFP coherence with tremor. Medial cerebellar nuclei and cerebellar vermis LFP coherence with tremor however remained unchanged from rest. These findings suggest harmaline-induced cerebellar oscillations are independent of behavioural state and associated changes in tremor amplitude. By contrast, thalamic oscillations are dependent on behavioural state and related changes in tremor amplitude. This study provides new insights into the role of cerebello-thalamo-cortical network interactions in tremor, whereby neural oscillations in thalamocortical, but not cerebellar circuits can be influenced by movement and/or behavioural tremor amplitude in the harmaline model.

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Proprioceptive thalamus receiving forelimb and neck muscle spindle inputs via the external cuneate nucleus in the rat

Cited by 20 publications

References 48 publications

A combinatorial input landscape in the “higher-order relay” posterior thalamic nucleus

A combinatorial input landscape in the “higher-order relay” posterior thalamic nucleus

Peripersonal encoding of forelimb proprioception in the mouse somatosensory cortex

Cerebello-Thalamo-Cortical Network Dynamics in the Harmaline Rodent Model of Essential Tremor

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