Presynaptic inhibition of spinal sensory feedback ensures smooth movement (original) (raw)
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The Journal of physiology, 2010
The intermediate zone of the spinal grey matter contains premotor interneurons mediating reflex actions of group I and II muscle afferents. However, limited information is available on how activity of inhibitory versus excitatory interneurons in this population are modulated and how they contribute to motor networks. There were three aims of this study: (1) to characterize excitatory axonal contacts on interneurons; (2) to determine if contact patterns on excitatory and inhibitory interneurons are different; (3) to determine if there are differences in presynaptic inhibitory control of excitatory and inhibitory interneurons. We used intracellular labelling of electrophysiologically identified cells along with immunochemistry to characterise contacts formed by axons that contain vesicular glutamate transporters (VGLUT1 and VGLUT2) and contacts formed by VGLUT1 terminals which in turn were contacted by GABAergic terminals on cells that were characterised according to their transmitter...
Journal of Neuroscience, 2011
Commissural inhibitory interneurons (INs) are integral components of the locomotor circuitry that coordinate left-right motor activity during movements. We have shown that GABA-mediated synaptic transmission plays a key role in generating alternating locomotor-like activity in the mouse spinal cord . The primary objective of our study was to determine whether properties of lamina VIII (LVIII) GABAergic INs in the spinal cord of GAD67::GFP transgenic mice fit the classification of rhythm-coordinating neurons in the locomotor circuitry. The relatively large GFP+ INs had comparable morphological and electrophysiological properties, suggesting that they comprised a homogenous neuronal population. They displayed multipolar and complex dendritic arbors in ipsilateral LVII-LVIII and their axonal projections crossed the ventral commissure and branched into contralateral ventral, medial and dorsal laminae. Putative synaptic contacts evident as bouton-like varicosities were detected in close apposition to lateral motoneurons, Renshaw cells, other GFP+ INs and unidentified neurons. Exposure to a rhythmogenic cocktail triggered locomotor-like rhythmic firing in the majority of LVIII GFP+ INs. Their induced oscillatory activity was out of phase with bursts of contralateral motoneurons and in phase with bouts of ipsilateral motor activity. Membrane voltage oscillations were elicited by rhythmic increases in excitatory synaptic drive and might have been augmented by three types of voltage-activated cationic currents known to increase neuronal excitability. Based on their axonal projections and activity pattern we propose that this population of GABAergic INs forms a class of local commissural inhibitory interneurons that are integral component of the locomotor circuitry.
Journal of Neuroscience, 2014
have received the most attention, so little is known about how less reliable command-like interneurons may contribute to program generation. We study two electrically coupled interneurons, cerebral-buccal interneuron-2 (CBI-2) and CBI-11, which activate feeding motor programs in the mollusk Aplysia californica. Earlier work indicated that, in rested preparations, CBI-2, a powerful activator of programs, can trigger ingestive and egestive programs. CBI-2 reliably generated ingestive patterns only when it was repeatedly stimulated. The ability of CBI-2 to trigger motor activity has been attributed to the two program-promoting peptides it contains, FCAP and CP2. Here, we show that CBI-11 differs from CBI-2 in that it contains FCAP but not CP2. Furthermore, it is weak in its ability to drive programs. On its own, CBI-11 is therefore less effective as a program activator. When it is successful, however, CBI-11 is an effective specifier of motor activity; that is, it drives mostly ingestive programs. Importantly, we found that CBI-2 and CBI-11 complement each other's actions. First, prestimulation of CBI-2 enhanced the ability of CBI-11 to drive programs. This effect appears to be partly mediated by CP2. Second, coactivation of CBI-11 with CBI-2 makes CBI-2 programs immediately ingestive. This effect may be mediated by specific actions that CBI-11 exerts on pattern-generating interneurons. Therefore, different classes of command-like neurons in a motor network may make distinct, but potentially complementary, contributions as either activators or specifiers of motor activity.
Sensory input to primate spinal cord is presynaptically inhibited during voluntary movement
Nature Neuroscience, 2003
During normal voluntary movements, re-afferent sensory input continuously converges on the spinal circuits that are activated by descending motor commands. This time-varying input must either be synergistically combined with the motor commands or be appropriately suppressed to minimize interference. The earliest suppression could be produced by presynaptic inhibition, which effectively reduces synaptic transmission at the initial synapse. Here we report evidence from awake, behaving monkeys that presynaptic inhibition decreases the ability of afferent impulses to affect postsynaptic neurons in a behaviorally dependent manner. Evidence indicates that cutaneous afferent input to spinal cord interneurons is inhibited presynaptically during active wrist movement, and this inhibition is effectively produced by descending commands. Our results further suggest that this presynaptic inhibition has appropriate functional consequences for movement generation and may underlie increases in perceptual thresholds during active movement.
Interneuronal relay in spinal pathways from proprioceptors
Progress in Neurobiology, 1992
Introduction 1. I. Aims of the review 1.2. Terminology 1.3. Abbreviations 2. Methodology 2.1. "Downstream" and "upstream" approaches 2.2. Identification of target cells and type of action 2.3. Identification of patterns of convergence 3. Location of neurones relaying information from proprioceptors 3.1. Distribution of first order interneurones 3.2. Distribution of last order interneurones 3.3. Distribution of different functional populations 4. General characteristics of neurones contacted by proprioceptors 4.1. Morphology 4.2. Effectiveness of activation 4.3. Multimodal input 4.4. Shared input 5. Functional subdivision 6. Interneuronal selection 6.1. Modulation of sensitivity of receptors 6.2. Gating of input from sensory fibres 6.3. Selection by descending systems 6.4. Selection by interneuronal interactions 6.5. Evidence for selection of interneuronal subpopulations during voluntary movements in man 7. Interneurones mediating Ia reciprocal inhibition of antagonists 7.1. Location and morphology 7.2. Excitatory input 7.3. Inhibitory control systems 7.4. Target cells 7.5. Internal organisation 7.6. Mode of action 7.7. Main functions 7.8. Pharmacology/histochemistry 8. Interneurones inhibiting synergists or exciting antagonists 9. Interneurones contributing to wider motor synergies 9.1. Interneurones with a dominating input from Ib afferents 9.1.
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.
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...
European Journal of Neuroscience, 2003
Axonal projections and neurotransmitters used by commissural interneurons mediating crossed actions of reticulospinal neurons were investigated in adult cats. Eighteen interneurons, located in or close to lamina VIM in midlumbar segments, that were monosynaptically excited by reticulospinal tract fibres and projected to contralateral motor nuclei were labelled by intracellular injection of tetramethylrhodamine-dextran and Neurobiotin. The nine most completely labelled interneurons were analysed with combined confocal and light microscopy. None of the stem axons gave off ipsilateral axon collaterals. Seven cells had axon collaterals that arborized in the contralateral grey matter in the ventral horn of the same segments. Transmitters were identified by using antibodies raised against vesicular glutamate transporters 1 and 2, glutamic acid decarboxylase and the glycine transporter 2. The axons of two cells were immunoreactive for the glycine transporter 2 and hence were glycinergic. Three cells were immunoreactive for the vesicular glutamate transporter 2 and hence were glutamatergic. None of the axons displayed immunoreactivity for glutamic acid decarboxylase. Electron microscopy of two cells revealed direct synaptic connections with motoneurons and other neurons. Axonal swellings of one neuron formed synapses with profiles in motor nuclei whereas those of the other formed synapses with other structures, including cell bodies in lamina VII. The results show that this population of commissural interneurons includes both excitatory and inhibitory cells that may excite or inhibit contralateral motoneurons directly. They may also influence the activity of motoneurons indirectly by acting through interneurons located outside motor nuclei in the contralateral grey matter but are unlikely to have direct actions on interneurons in the ipsilateral grey matter.
Fast-Spiking Interneurons of the Premotor Cortex Contribute to Action Planning
SSRN Electronic Journal, 2021
Planning and execution of voluntary movement depend on the contribution of distinct classes of neurons in primary motor and premotor areas. However, the specific functional role of GABAergic cells remains only partly understood. Here, electrophysiological and computational analyses are employed to compare directly the response properties of putative pyramidal (PNs) and fast-spiking, GABAergic neurons (FSNs) during licking and forelimb retraction in mice. Recordings from anterolateral motor cortex and rostral forelimb area, reveal that FSNs fire earlier and for a longer duration than PNs, with the exception of a subset of early-modulated PNs in deep layers. Computational analysis reveals that FSNs carry vastly more information than PNs about the onset of movement. While PNs differently modulate their discharge during distinct motor acts, most FSNs respond with a stereotyped increase in firing rate. Accordingly, the informational redundancy was greater among FSNs than PNs. These data suggest that a global rise of inhibition contributes to early action planning.