In the back of your mind: Cortical mapping of tactile and proprioceptive paraspinal afferent inputs

Persistent pain alters brain-body representations, highlighting their potential pathological significance. In chronic low back pain (LBP), sparse evidence points towards a shift of the cortical representation of sensory afferents of the back. However, systematic investigations of the cortical representation of tactile and proprioceptive paraspinal afferents along the thoracolumbar axis are lacking. Detailed cortical maps of paraspinal afferent input might be crucial to further explore potential relationships between brain changes and the development and maintenance of chronic LBP. We therefore validated a novel and functional magnetic resonance imaging- (fMRI-)compatible method of mapping cortical representations of tactile and proprioceptive afferents of the back, using pneumatic vibrotactile stimulation ("pneuVID") at varying frequencies and paraspinal locations, in conjunction with high-resolution fMRI. We hypothesised that: (i) high (80 Hz) frequency stimulation would lead to increased postural sway compared to low (20 Hz) stimulation, due to differential evoked mechanoreceptor contributions to postural control (proprioceptive vs tactile); and (ii) that high (80 Hz) versus low (20 Hz) frequency stimulation would be associated with neuronal activity in distinct primary somatosensory (S1) and motor (M1) cortical targets of tactile and proprioceptive afferents (N=15, healthy volunteers). Additionally, we expected neural representations to vary spatially along the thoracolumbar axis. We found significant differences between neural representations of low and high frequency stimulation and between representations of thoracic and lumbar paraspinal locations, in several bilateral sensorimotor cortical regions. Proprioceptive (80 Hz) stimulation preferentially activated sub-regions S1 3a and M1 4p, while tactile (20 Hz) stimulation was more encoded in S1 3b and M1 4a. Moreover, in S1, lower back proprioceptive stimulation activated dorsal-posterior representations, compared to ventral-anterior representations activated by upper back stimulation. As per our hypotheses, we found distinct sensorimotor cortical tactile and proprioceptive representations, with the latter displaying clear topographic differences between the upper and lower back. This thus represents the first behavioural and neurobiological validation of the novel pneuVID method for stimulating muscle spindles and mapping cortical representations of paraspinal afferents. Future investigations of detailed cortical maps will be of major importance in elucidating the role of cortical reorganization in the pathophysiology of chronic LBP.

Disruption of Proprioceptive Information During Electrical Stimulation of the Cutaneous Afferents

Restoration of proprioception with neurotechnology is critical to improve effectiveness of robotic neuro-prostheses. Unfortunately, after initial enthusiasm clinical results showed that unlike touch, proprioception could not be reliably induced. Here we show that concurrent activation of multiple sensory modalities may trigger unwanted sensory regulation mechanisms that disrupt proprioception. We recorded intra-spinal neural activity induced by stimulation of proprioceptive afferents from the radial nerve in three monkeys. Then, we superimposed stimulation of the radial nerve cutaneous branch and quantified its impact on spinal neural activity via population analysis. Proprioceptive pulses produced robust neural trajectories in the neural manifold that were disrupted by concurrent stimulation of cutaneous afferents. This disruption correlated with a reduction of afferent volleys and multi-unit activity both in the spinal cord and somatosensory cortex. Our results suggest that limited specificity not only impacts localization of artificial percepts, but also their nature to an extent that was never considered.

Disruption Of Proprioceptive Information During Electrical Stimulation Of The Cutaneous Afferents

Restoration of proprioception with neurotechnology is critical to improve effectiveness of robotic neuro-prostheses. Unfortunately, after initial enthusiasm clinical results showed that unlike touch, proprioception could not be reliably induced. Here we show that concurrent activation of multiple sensory modalities may trigger unwanted sensory regulation mechanisms that disrupt proprioception. We recorded intra-spinal neural activity induced by stimulation of proprioceptive afferents from the radial nerve in three monkeys. Then, we superimposed stimulation of the radial nerve cutaneous branch and quantified its impact on spinal neural activity via population analysis. Proprioceptive pulses produced robust neural trajectories in the neural manifold that were disrupted by concurrent stimulation of cutaneous afferents. This disruption correlated with a reduction of afferent volleys and multi-unit activity both in the spinal cord and somatosensory cortex. Our results suggest that limited specificity not only impacts localization of artificial percepts, but also their nature to an extent that was never considered.

Proprioceptive afferents differentially contribute to effortful perception of object heaviness and mass distribution

When humans handle a tool, such as a tennis racket or hammer, for the first time, they often wield it to determine its inertial properties, however, the mechanisms that contribute to perception of inertial properties are not fully understood. The goal of the present study was to investigate how proprioceptive afferents contribute to effortful perception of heaviness and mass distribution of a manually wielded object in the absence of vision. Blindfolded participants manually wielded a set of specially-designed experimental objects of different mass and mass distribution about the wrist at different wrist angles and wrist angular kinematics. By independently manipulating these variables, we aimed to elicit different levels of tonic and rhythmic activity in the muscle spindles of the wrist flexors and extensors and relate them to reported perceptual judgments of heaviness and length. Perception of heaviness and length were predominantly dependent on an object’s static moment and the moment of inertia, respectively. Manipulations of wrist angle and wrist angular kinematics affected perceptual judgments of heaviness and length in relatively opposite ways. As for wrist angle, ulnar deviation consistently resulted in an object being perceived heavier but shorter. Compared to static holding, wielding the object resulted in it being perceived heavier but wielding did not affect perceived length. These results suggest that proprioceptive afferents differentially contribute to effortful perception of object heaviness and mass distribution.

A New System to Objectively Measure Ankle Proprioception

Proprioceptive afferents from the ankle joint are essential feedback for maintaining balance. However, there is no widely accepted test or measurement system available for determining the proprioceptive accuracy of the human ankle joint. Here, we present a system with a novel hardware design that applies an established psychometric testing protocol that generates a Just-Noticeable-Difference (JND) threshold as a measure of ankle proprioceptive acuity at the end of testing. To establish the system validity, twelve healthy adult participants completed the assessment. Testing required 25 trials and took approximately 10 minutes to complete. We show exemplar data of the ankle JND threshold and the summary results for all twelve participants. This assessment has the potential to become a tool for clinicians to identify proprioceptive impairment at the ankle and to assess the efficacy of sensorimotor interventions for improving balance in clinical populations.

Proprioceptive Stimulation of the Articulatory Muscles for Restoration of Speech and Swallowing

Objective of the Paper: To assess the possibility of supplementing standard speech therapy protocols for dysarthria patients in the acute period of ischemic stroke, with techniques for stimulating the afferent nerves of the mouth and articulatory organs via a proprietary training mask designed to improve proprioception. Key Points: The paper describes a clinical case of using the training mask. Repeated speech evaluations and changes in scores on scales for assessing the severity of speech problems and dysarthria showed that stimulation of the proprioceptive afferents in the mouth and articulatory organs improved mimetic muscle function and speech articulation, contributed to normalizing muscle tone in the articulatory muscles, and reduced speech hesitation. Conclusion: The clinical case described in the paper demonstrates the positive effects of a training mask designed for proprioceptive stimulation of the articulatory muscles in patients with acute ischemic stroke. These results will be of interest to neurologists, speech therapists, and specialists in neurorehabilitation. Keywords: dysarthria, pseudobulbar disorders, extrapyramidal disorders, training mask, ischemic stroke.

Proprioceptive Recognition with Artificial Neural Networks Based on Organizations of Spinocerebellar Tract and Cerebellum

Muscle kinematics and kinetics are nonlinearly encoded by proprioceptors, and the changes in muscle length and velocity are integrated into Ia afferent. Besides, proprioceptive signals from multiple muscles are probably mixed in afferent pathways, which all lead to difficulties in proprioceptive recognition for the cerebellum. In this study, the artificial neural networks, whose organizations are biologically based on the spinocerebellar tract and cerebellum, are utilized to decode the proprioceptive signals. Consistent with the controversy of the proprioceptive division in the dorsal spinocerebellar tract, the spinocerebellar tract networks incorporated two distinct inferences, (1) the centralized networks, which mixed Ia, II, and Ib and processed them together; (2) the decentralized networks, which processed Ia, II, and Ib afferents separately. The cerebellar networks were based on the Marr–Albus model to recognize the kinematic states. The networks were trained by a specific movement, and the trained networks were subsequently required to predict kinematic states of six movements. The results demonstrated that the centralized networks, which were more consistent with the physiological findings in recent years, had better recognition accuracy than the decentralized networks, and the networks were still effective even when proprioceptive afferents from multiple muscles were integrated.

Extrasynaptic α5GABAA receptors on proprioceptive afferents produce a tonic depolarization that modulates sodium channel function in the rat spinal cord

Activation of GABAA receptors on sensory axons produces a primary afferent depolarization (PAD) that modulates sensory transmission in the spinal cord. While axoaxonic synaptic contacts of GABAergic interneurons onto afferent terminals have been extensively studied, less is known about the function of extrasynaptic GABA receptors on afferents. Thus, we examined extrasynaptic α5GABAA receptors on low-threshold proprioceptive (group Ia) and cutaneous afferents. Afferents were impaled with intracellular electrodes and filled with neurobiotin in the sacrocaudal spinal cord of rats. Confocal microscopy was used to reconstruct the afferents and locate immunolabelled α5GABAA receptors. In all afferents α5GABAA receptors were found throughout the extensive central axon arbors. They were most densely located at branch points near sodium channel nodes, including in the dorsal horn. Unexpectedly, proprioceptive afferent terminals on motoneurons had a relative lack of α5GABAA receptors. When recording intracellularly from these afferents, blocking α5GABAA receptors (with L655708, gabazine, or bicuculline) hyperpolarized the afferents, as did blocking neuronal activity with tetrodotoxin, indicating a tonic GABA tone and tonic PAD. This tonic PAD was increased by repeatedly stimulating the dorsal root at low rates and remained elevated for many seconds after the stimulation. It is puzzling that tonic PAD arises from α5GABAA receptors located far from the afferent terminal where they can have relatively little effect on terminal presynaptic inhibition. However, consistent with the nodal location of α5GABAA receptors, we find tonic PAD helps produce sodium spikes that propagate antidromically out the dorsal roots, and we suggest that it may well be involved in assisting spike transmission in general. NEW & NOTEWORTHY GABAergic neurons are well known to form synaptic contacts on proprioceptive afferent terminals innervating motoneurons and to cause presynaptic inhibition. However, the particular GABA receptors involved are unknown. Here, we examined the distribution of extrasynaptic α5GABAA receptors on proprioceptive Ia afferents. Unexpectedly, these receptors were found preferentially near nodal sodium channels throughout the afferent and were largely absent from afferent terminals. These receptors produced a tonic afferent depolarization that modulated sodium spikes, consistent with their location.