Identification of a Spinal Circuit for Light Touch and Fine Motor Control (original) (raw)

Genetically identified spinal interneurons integrating tactile afferents for motor control

Journal of Neurophysiology, 2015

Our movements are shaped by our perception of the world as communicated by our senses. Perception of sensory information has been largely attributed to cortical activity. However, a prior level of sensory processing occurs in the spinal cord. Indeed, sensory inputs directly project to many spinal circuits, some of which communicate with motor circuits within the spinal cord. Therefore, the processing of sensory information for the purpose of ensuring proper movements is distributed between spinal and supraspinal circuits. The mechanisms underlying the integration of sensory information for motor control at the level of the spinal cord have yet to be fully described. Recent research has led to the characterization of spinal neuron populations that share common molecular identities. Identification of molecular markers that define specific populations of spinal neurons is a prerequisite to the application of genetic techniques devised to both delineate the function of these spinal neur...

Presynaptic inhibition of spinal sensory feedback ensures smooth movement

Nature, 2014

The precision of skilled movement depends on sensory feedback and its refinement by local inhibitory microcircuits. One specialized set of spinal GABAergic interneurons forms axo-axonic contacts with the central terminals of sensory afferents, exerting presynaptic inhibitory control over sensory-motor transmission. The inability to achieve selective access to the GABAergic neurons responsible for this unorthodox inhibitory mechanism has left unresolved the contribution of presynaptic inhibition to motor behavior. We used Gad2 as a genetic entry point to manipulate the interneurons that contact sensory terminals, and show that activation of these interneurons in mice elicits the defining physiological characteristics of presynaptic inhibition. Selective genetic ablation of Gad2-expressing interneurons severely perturbs goal-directed reaching movements, uncovering a pronounced and stereotypic forelimb motor oscillation, the core features of which are captured by modeling the consequences of sensory feedback at high gain. Our findings define the neural substrate of a genetically hard-wired gain control system crucial for the smooth execution of movement. Animals execute skilled limb movements with seemingly effortless precision, belying an elaborate series of neural transformations that direct each motor act. Spinal motor output relies on local inhibitory interneurons that shape the response of motor neurons to diverse excitatory inputs 1. Most inhibitory interneurons form direct postsynaptic connections with motor or premotor neurons 2 , but a small subset of GABAergic interneurons instead forms Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use:

Circuits for Grasping: Spinal dI3 Interneurons Mediate Cutaneous Control of Motor Behavior

Neuron, 2013

Accurate motor performance depends on the integration in spinal microcircuits of sensory feedback information. Hand grasp is a skilled motor behavior known to require cutaneous sensory feedback, but spinal microcircuits that process and relay this feedback to the motor system have not been defined. We sought to define classes of spinal interneurons involved in the cutaneous control of hand grasp in mice and to show that dI3 interneurons, a class of dorsal spinal interneurons marked by the expression of Isl1, convey input from low threshold cutaneous afferents to motoneurons. Mice in which the output of dI3 interneurons has been inactivated exhibit deficits in motor tasks that rely on cutaneous afferent input. Most strikingly, the ability to maintain grip strength in response to increasing load is lost following genetic silencing of dI3 interneuron output. Thus, spinal microcircuits that integrate cutaneous feedback crucial for paw grip rely on the intermediary role of dI3 interneurons.

Nerve-Specific Input Modulation to Spinal Neurons during a Motor Task in the Monkey

The Journal of Neuroscience, 2017

If not properly regulated, the large amount of reafferent sensory signals generated by our own movement could destabilize the CNS. We investigated how input from peripheral nerves to spinal cord is modulated during behavior. We chronically stimulated the deep radial nerve (DR; proprioceptive, wrist extensors), the median nerve (M; mixed, wrist flexors and palmar skin) and the superficial radial nerve (SR; cutaneous, hand dorsum) while four monkeys performed a delayed wrist flexion-extension task. Spinal neurons putatively receiving direct sensory input were defined based on their evoked response latency following nerve stimulation. We compared the influence of behavior on the evoked response (responsiveness to a specific peripheral input) and firing rate of 128 neuron-nerve pairs based on their source nerve. Firing rate increased during movement regardless of source nerve, whereas evoked response modulation was strikingly nerve-dependent. In SR (n ϭ 47) and M (n ϭ 27) neurons (cutaneous or mixed input), the evoked response was suppressed during wrist flexion and extension. In contrast, in DR neurons (n ϭ 54, pure proprioceptive input), the evoked response was facilitated exclusively during movements corresponding to the contraction of DR spindle-bearing muscles (i.e., wrist extension). Furthermore, modulations of firing rate and evoked response were uncorrelated in SR and M neurons, whereas they tended to be positively comodulated in DR neurons. Our results suggest that proprioceptive and cutaneous inputs to the spinal cord are modulated differently during voluntary movements, suggesting a refined gating mechanism of sensory signals according to behavior.

In Vivo Interrogation of Spinal Mechanosensory Circuits

Cell Reports, 2016

Highlights d A system for optogenetic control of spinal circuits using offthe-shelf components d Bidirectional control of SOM+ neurons indicates primary role in mechanosensation d Temporally sparse SOM+ neuron stimulation reveals role in itch sensation

A spinal organ of proprioception for integrated motor action feedback

Neuron, 2021

Highlights d A central organ of proprioception exists in the spinal cord d Piezo2-expressing mechanosensitive neurons sense lateral bending of spinal cord d These are inhibitory commissural neurons targeting the locomotor rhythm generator d Intraspinal proprioceptive feedback aligns movements with motor commands

Motor Control in the Human Spinal Cord

Artificial Organs, 2005

Features of the human spinal cord motor control are described using two spinal cord injury models: (i) the spinal cord completely separated from brain motor structures by accidental injury; (ii) the spinal cord receiving reduced and altered supraspinal input due to an incomplete lesion. Systematic studies using surface electrode polyelectromyography were carried out to assess skeletal muscle reflex responses to single and repetitve stimulation in a large number of subjects. In complete spinal cord injured subjects the functional integrity of three different neuronal circuits below the lesion level is demonstrated: first, simple mono-and oligosynaptic reflex arcs and polysynaptic pathways; second, propriospinal interneuron system with their cell in the gray matter and the axons in the white matter of the spinal cord conducting activity between different spinal cord segments; and third, internuncial gray matter neurons with short axons and dense neuron contact within the spinal gray matter. All of these three systems participate continuously in the generation of

Propagation of Sinusoidal Electrical Waves along the Spinal Cord during a Fictive Motor Task

Journal of Neuroscience, 2009

We present for the first time direct electrophysiological evidence of the phenomenon of traveling electrical waves produced by populations of interneurons within the spinal cord. We show that, during a fictive rhythmic motor task, scratching, an electrical field potential of spinal interneurons takes the shape of a sinuous wave, "sweeping" the lumbosacral spinal cord rostrocaudally with a mean speed of ϳ0.3 m/s. We observed that traveling waves and scratching have the same cycle duration and that duration of the flexor phase, but not of the extensor phase, is highly correlated with the cycle duration of the traveling waves. Furthermore, we found that the interneurons from the deep dorsal horn and the intermediate nucleus can generate the spinal traveling waves, even in the absence of motoneuronal activity. These findings show that the sinusoidal field potentials generated during fictive scratching could be a powerful tool to disclose the organization of central pattern generator networks.