Long-Distance Descending Spinal Neurons Ensure Quadrupedal Locomotor Stability

Ruder, Ludwig; Takeoka, Aya; Arber, Silvia

doi:10.1016/j.neuron.2016.10.032

Cited by 111 publications

(171 citation statements)

References 63 publications

(87 reference statements)

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“…One role of ipsilateral inhibition is to mediate flexor-extensor alternations via Ia reciprocal inhibition from V2b and V1 populations [18, 19]. Ipsilaterally descending propriospinal neurons may also stabilize left-right alternation, although specific ablation of inhibitory ipsilaterally descending neurons has not been tested [8, 59]. Our work establishes that selective suppression of V2b activity increases tail beat frequency (Fig.…”

Section: Discussionsupporting

confidence: 57%

Spinal V2b neurons reveal a role for ipsilateral inhibition in speed control

Callahan¹,

Roberts²,

Sengupta³

et al. 2019

Preprint

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10The spinal cord contains a diverse array of interneurons that govern motor output. Traditionally, 11 models of spinal circuits have emphasized the role of inhibition in enforcing reciprocal 12 alternation between left and right sides or flexors and extensors. However, recent work has 13shown that inhibition also increases coincident with excitation during contraction. Here, using 14 larval zebrafish, we investigate the V2b (Gata3+) class of neurons, which contribute to flexor-15 extensor alternation but are otherwise poorly understood. Using newly generated transgenic lines 16 we define two stable subclasses with distinct neurotransmitter and morphological properties. 17These two V2b subclasses make direct synapses onto motor neurons with differential targeting to 18 slower and faster circuits. In vivo, optogenetic suppression of V2b activity leads to increases in 19 locomotor speed. We conclude that V2b neurons exert speed-specific influence over axial motor 20 circuits throughout the rostrocaudal axis. Together, these results indicate a new role for 21 ipsilateral inhibition in speed control. 22 46In-phase inhibition is thought to derive from two spinal interneuron classes, the V1 and V2b 47 populations. The V1 population includes Renshaw cells [15, 16], which provide recurrent 48 inhibition onto motor neurons with potentially significant shunting effects [17]. To date, most 49 analysis of drive from V2b neurons has focused on the shared contributions of V1s and V2bs to 50 reciprocal inhibition governing flexor/extensor alternation in limbed animals [18][19][20]. However, 51 this does not shed light on potential functions of ipsilateral inhibition in gain control for 52 regulation of motor neuron firing during contraction, as opposed to suppression of motor neuron 53 firing during extension. 54 55In-phase inhibition increases in amplitude for faster locomotor movements [10] suggesting a 56 potential role in speed control. Here we investigated whether V2b neurons could indeed provide 57 direct inhibition to motor neurons for speed control, taking advantage of the speed-dependent 58 organization of zebrafish motor circuits [21][22][23]. V2b neurons are good candidates for in-phase 59 gain control because they are exclusively inhibitory in mouse and zebrafish [24] with ipsilateral, 60 descending axons within the spinal cord [18, 25]. They arise from a final progenitor division that 61 produces pairs of V2a and V2b neurons [26]. Given the role of V2a neurons in triggering motor 62 output [27, 28], particularly through speed-specific circuits for titrating levels of motor excitation 63[4, 29-31], it seems plausible that their sister V2b neurons exert an opposing, inhibitory role in 64 speed control. However, the V2b class has not been well characterized at anatomical or 65 neurochemical levels outside of very early development. 66 67 5Here, we define two subclasses of V2b neurons in larval zebrafish based on differential 68 transmitter expression and anatomy, and further show that these neurons directly inhibit a...

show abstract

Section: Discussionsupporting

confidence: 57%

Spinal V2b neurons reveal a role for ipsilateral inhibition in speed control

Callahan¹,

Roberts²,

Sengupta³

et al. 2019

Preprint

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show abstract

“…Reticulospinal systems control adult body and eye movements (Sparks, 2002;Dubuc et al 2008;Jordan et al 2008;Arber, 2012;Ruder et al 2016) but it is the mammal cortical decision circuits, which act as higher level control systems, that have been studied in such detail (Hanes & Schall, 1996;Schall, 2003;Smith & Ratcliff, 2004). Our findings suggest that at early stages of development in tadpoles and fish (Kimura et al 2013) decisions are made in reticulospinal neurons in the brainstem.…”

Section: How Do Our Findings In the Tadpole Relate To Models Of Decismentioning

confidence: 76%

“…; Arber, ; Ruder et al . ) but it is the mammal cortical decision circuits, which act as higher level control systems, that have been studied in such detail (Hanes & Schall, ; Schall, ; Smith & Ratcliff, ). Our findings suggest that at early stages of development in tadpoles and fish (Kimura et al .…”

Section: Discussionmentioning

confidence: 99%

A simple decision to move in response to touch reveals basic sensory memory and mechanisms for variable response times

Koutsikou

Merrison-Hort

Buhl

et al. 2018

The Journal of Physiology

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Many motor responses to sensory input, like locomotion or eye movements, are much slower than reflexes. Can simpler animals provide fundamental answers about the cellular mechanisms for motor decisions? Can we observe the 'accumulation' of excitation to threshold proposed to underlie decision making elsewhere? We explore how somatosensory touch stimulation leads to the decision to swim in hatchling Xenopus tadpoles. Delays measured to swimming in behaving and immobilised tadpoles are long and variable. Activity in their extensively studied sensory and sensory pathway neurons is too short-lived to explain these response delays. Instead, whole-cell recordings from the hindbrain reticulospinal neurons that drive swimming show that these receive prolonged, variable synaptic excitation lasting for nearly a second following a brief stimulus. They fire and initiate swimming when this excitation reaches threshold. Analysis of the summation of excitation requires us to propose extended firing in currently undefined presynaptic hindbrain neurons. Simple models show that a small excitatory recurrent-network inserted in the sensory pathway can mimic this process. We suggest that such a network may generate slow, variable summation of excitation to threshold. This excitation provides a simple memory of the sensory stimulus. It allows temporal and spatial integration of sensory inputs and explains the long, variable delays to swimming. The process resembles the 'accumulation' of excitation proposed for cortical circuits in mammals. We conclude that fundamental elements of sensory memory and decision making are present in the brainstem at a surprisingly early stage in development.

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“…While neuronal mechanisms involved in left-right coordination of hindlimbs are mostly driven by segmental spinal neurons and fairly well understood (Kiehn, 2016), much less is known about circuit mechanisms for foreand hindlimb coordination. A recent study demonstrated that long projection neurons interconnecting the cervical and lumbar spinal cord are important in coordinating fore-and hindlimb patterns during high-speed locomotion as well as for maintenance of postural stability ( Figure 2C) (Ruder et al, 2016). The characterized long projection neurons are composed of a major excitatory and a minor inhibitory population derived from distinct developmental origin, each establishing specific projection patterns ( Figure 2C).…”

Section: Neuronmentioning

confidence: 96%

Connecting Circuits for Supraspinal Control of Locomotion

Ferreira‐Pinto¹,

Ruder²,

Capelli³

et al. 2018

Neuron

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117

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Locomotion is regulated by distributed circuits and achieved by the concerted activation of body musculature. While the basic properties of executive circuits in the spinal cord are fairly well understood, the precise mechanisms by which the brain impacts locomotion are much less clear. This Review discusses recent work unraveling the cellular identity, connectivity, and function of supraspinal circuits. We focus on their involvement in the regulation of the different phases of locomotion and their interaction with spinal circuits. Dedicated neuronal populations in the brainstem carry locomotor instructions, including initiation, speed, and termination. To align locomotion with behavioral needs, brainstem output structures are recruited by midbrain and forebrain circuits that compute and infer volitional, innate, and context-dependent locomotor properties. We conclude that the emerging logic of supraspinal circuit organization helps to understand how locomotor programs from exploration to hunting and escape are regulated by the brain.

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Long-Distance Descending Spinal Neurons Ensure Quadrupedal Locomotor Stability

Cited by 111 publications

References 63 publications

Spinal V2b neurons reveal a role for ipsilateral inhibition in speed control

Spinal V2b neurons reveal a role for ipsilateral inhibition in speed control

A simple decision to move in response to touch reveals basic sensory memory and mechanisms for variable response times

Connecting Circuits for Supraspinal Control of Locomotion

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