The Positional Logic of Sensory-Motor Reflex Circuit Assembly

Balaskas, Nikolaos; Ng, David Chee Eng; Zampieri, Niccolò

doi:10.1016/j.neuroscience.2020.04.038

Cited by 10 publications

(7 citation statements)

References 70 publications

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“…These findings support the idea that individual mXns develop specific input connectivity that is appropriate for their innervation targets, independent of their positioning. This is different from the positional strategy proposed for mammalian spinal motor neurons, in which motor neurons with common targets receive sensory input based on their distinct clustered positions in the spinal cord 5,34 . To directly test whether mXns can develop specific input connectivity irrespective of their position in the topographic map, we manipulated mXn positions through transplantation.…”

Section: 21mentioning

confidence: 77%

“…How are these intermingled diverse motor neurons incorporated in neural networks? A positional strategy such as occurs in limb-innervating motor neurons, where the position of motor neurons determines which presynaptic neurons they connect to [19][20][21][22] , would likely cause neighboring vagus motor neurons to connect with common presynaptic neurons, making functionally heterogenous groups of neurons fire together. It is an open question whether, and how, adjacent neurons with different functions can be activated differently for sophisticated peripheral control.…”

Section: Introductionmentioning

confidence: 99%

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Position-independent functional refinement within the vagus motor topographic map

Kaneko,

Boulanger-Weill,

Isabella

et al. 2023

Preprint

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The vagus nerve (10thcranial nerve) mediates brain-body communication by innervating and controlling various internal body parts, including the pharynx, larynx, and most visceral organs. Vagus sensory neurons send information about internal states to the brain, and vagus motor neurons return reflexive motor responses, such as gagging, swallowing, digestive enzyme secretion, gut peristalsis and heart rate adjustment. The diverse motor neurons underlying these bodily functions are topographically organized in the brainstem. However, the topographic map is continuous, with motor neurons innervating a common target, a “target group”, partly intermingled with neurons of other target groups, without clear boundaries. Particularly, motor neurons supplying different pharyngeal muscles are significantly overlapping in the topographic map throughout vertebrates. It remains unanswered how this intermingled diverse population of motor neurons can control different bodily functions. Through calcium imaging in larval zebrafish, we demonstrate that, when noxious stimulation is given focally to the larval pharynx, vagus motor neurons return stereotypic muscle activity patterns appropriate for the location of the stimulus. We show that vagus motor neurons that produce pharyngeal contraction following focal noxious stimulation are loosely distributed in the motor nucleus, consistent with the loose and overlapping distribution of anatomical target groups. This suggests that the connectivity of motor neurons is determined at the single-neuron level, not the neighboring population level. Remarkably, we show that pharynx-innervating motor neurons can maintain their appropriate response patterns to focal noxious stimulation even when their topographic organization is disrupted, and that mis-positioned motor neurons elaborate dendrites that extend towards the dendritic territory of their target group. We further identified that the motor activity patten is immature when motor neurons first initiate sensory-evoked responses and that maturation, dendrite extension and incorporation into the correct sensory motor circuit all depend on the efficiency of neurotransmission from the motor axons. Our data together suggest a position-independent wiring strategy that refines presynaptic connectivity of motor neurons through experience-dependent feedback regulation. We further demonstrate resilience to topographic manipulation in viscera-innervating vagus motor neurons, supporting that position-independent wiring is a general principle.

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Section: 21mentioning

confidence: 77%

Section: Introductionmentioning

confidence: 99%

Position-independent functional refinement within the vagus motor topographic map

Kaneko,

Boulanger-Weill,

Isabella

et al. 2023

Preprint

View full text Add to dashboard Cite

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“…Expression of the TVA receptor and G are required for selective infection by EnvA pseudotyped G-deleted RV (RVΔG-mCherry/EnvA) and subsequent monosynaptic spreading, while the nuclear GFP reporter allows identification of starter cells (Figure 1A). We first focused on proprioceptive circuits that have been quite extensively characterized at anatomical and physiological levels (Zampieri et al, 2014; Balaskas et al, 2020). Thus, we crossed parvalbumin::Cre ( PV::Cre ), which is expressed in proprioceptive sensory neurons and a subset of low-threshold mechanoreceptors (LTMR) with the HTB mouse line (Hippenmeyer et al, 2007; de Nooij et al, 2013).…”

Section: Resultsmentioning

confidence: 99%

Rabies anterograde monosynaptic tracing reveals organization of spinal sensory circuits

Pimpinella

Zampieri

2021

Preprint

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Somatosensory neurons detect vital information about the environment and internal status of the body, such as temperature, touch, itch and proprioception. The circuit mechanisms controlling the coding of somatosensory information and the generation of appropriate behavioral responses are not clear yet. In order to address this issue, it is important to define the precise connectivity patterns between primary sensory afferents dedicated to the detection of different stimuli and recipient neurons in the central nervous system. In this study we used a rabies tracing approach for mapping spinal circuits receiving sensory input from distinct, genetically defined, modalities. We analyzed the anatomical organization of spinal circuits involved in coding of thermal and mechanical stimuli and showed that somatosensory information from distinct modalities is relayed to partially overlapping ensembles of interneurons displaying stereotyped laminar organization, thus highlighting the importance of positional features and population coding for the processing and integration of somatosensory information.

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“…Proprioceptive sensory neurons can be anatomically and functionally divided on the basis of the identity of the muscle and receptor organ they innervate. First, during early development, proprioceptors innervate muscles and in order to precisely adjust motor output according to the biomechanical properties of their targets wire with neural circuits in the central nervous system (CNS) with exquisite specificity 2 , 3 . In addition, at a receptor level, proprioceptors can be further distinguished into three subtypes - Ia, Ib, and II - by their selective contribution to either muscle spindles (MS; Ia and II) or Golgi tendon organs (GTO; Ib) 4 .…”

Section: Introductionmentioning

confidence: 99%

Molecular identity of proprioceptor subtypes innervating different muscle groups in mice

et al. 2022

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The precise execution of coordinated movements depends on proprioception, the sense of body position in space. However, the molecular underpinnings of proprioceptive neuron subtype identities are not fully understood. Here we used a single-cell transcriptomic approach to define mouse proprioceptor subtypes according to the identity of the muscle they innervate. We identified and validated molecular signatures associated with proprioceptors innervating back (Tox, Epha3), abdominal (C1ql2), and hindlimb (Gabrg1, Efna5) muscles. We also found that proprioceptor muscle identity precedes acquisition of receptor character and comprise programs controlling wiring specificity. These findings indicate that muscle-type identity is a fundamental aspect of proprioceptor subtype differentiation that is acquired during early development and includes molecular programs involved in the control of muscle target specificity.

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The Positional Logic of Sensory-Motor Reflex Circuit Assembly

Cited by 10 publications

References 70 publications

Position-independent functional refinement within the vagus motor topographic map

Position-independent functional refinement within the vagus motor topographic map

Rabies anterograde monosynaptic tracing reveals organization of spinal sensory circuits

Molecular identity of proprioceptor subtypes innervating different muscle groups in mice

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