Proprioceptive population coding of two-dimensional limb movements in humans: I. Muscle spindle feedback during spatially oriented movements

Abstract

The proprioceptive coding of multidirectional ankle joint movements was investigated, focusing in particular on the question as to how accurately the direction of a movement is encoded when all the proprioceptive information from all the muscles involved in the actual movement is taken into account. During ankle movements imposed on human subjects, the activity of 30 muscle spindle afferents originating in the extensor digitorum longus, tibialis anterior, extensor hallucis longus and peroneus lateralis muscles was recorded from the lateral peroneal nerve using the microneurographic technique. In the first part of the study, it was proposed to investigate whether muscle spindle afferents have a preferred direction, as previously found to occur in the case of cortical cells, and to analyze the neural coding of the movement trajectories using a "population vector model." This model is based on the idea that neuronal coding can be analyzed in terms of a series of vectors, each based on specific movement parameters. In the present case, each vector gives the mean contribution of a population of muscle spindle afferents within one directionally tuned muscle. A given population vector points in the "preferred sensory direction" of the muscle to which it corresponds, and its length is the mean frequency of all the afferents within that muscle. Our working hypothesis was that the sum of these weighted vectors points in the same direction as the ongoing movement. The results show that each muscle spindle afferent, and likewise each muscle, has a specific preferred sensory direction, as well as a preferred sensory sector within which it is capable of sending sensory information to the central nervous system. Interestingly, the results also demonstrate that the preferred directions are the same as the directions of vibration-induced illusions. In addition, the results show that the neuronal population vector model describes the multipopulation proprioceptive coding of spatially oriented 2D limb movements, even at the peripheral sensory level, based on the sum vectors calculated from all the muscles involved in the movement. In an accompanying paper, the coding of more complex 2D movements such as those involved in drawing rectilinear and curvilinear geometrical shapes was investigated.

Fusimotor Drive May Adjust Muscle Spindle Feedback to Task Requirements in Humans

“…The right foot was laid on a stationary plate, and the left foot was attached to a rotating pedal connected to a computer-controlled machine. This movable machine allowed two-dimensional movements to be imposed (see Bergenheim et al 2000). On the front plane of the machine (y, vertical axe), a downward (90°) or upward (270°) movement created a plantar flexion or dorsiflexion of the ankle joint, respectively.…”

“…A sideward movement (x, horizontal axe) to the left (180°) or to the right (0°) resulted in an eversion or inversion of the foot, respectively. Here ramp-and-hold movements were imposed in the preferred sensory direction of the receptor-bearing muscle, i.e., 59, 73, 96, and 311°for afferents belonging to EDL, EHL, TA, and PL muscles, respectively (see Bergenheim et al 2000). The components of each movement along the horizontal (x) and vertical (y) axes were sampled at 100 Hz.…”

Effects of experimentally‐induced anterior knee pain on knee joint position sense in healthy individuals

“…At the ankle joint it has been shown that muscle spindle information from several muscles contributes to ankle proprioception [5]. It has been suggested that a large distribution of pain can interfere with proprioception by disturbing a large number of muscle spindles.…”

Inducing Any Virtual Two-Dimensional Movement in Humans by Applying Muscle Tendon Vibration

“…First, microneurography serves to record feedback messages triggered in populations of afferents from all the muscles surrounding a given joint in response to two-dimensional movements performed under active and passive conditions Cordo et al 2002;Jones et al 2001;Roll et al 2000Roll et al , 2004. In addition, the "population vector model," first used at the cortical level (Georgopoulos 1982), was adapted to ensembles of somesthetic sensory neurons and to the particular anatomical and physiological organization of the cutaneous and muscular systems (Aimonetti et al 2007;Bergenheim et al 2000;Jones et al 2001;Roll et al 2000). Indeed, the muscle spindles merge into a very homogeneous population inside the muscle that bears them.…”

“…The direction of this population vector is the Preferred Sensory Direction of a given muscle (i.e., the average of the preferred sensory directions of all the muscle spindles in that muscle), whereas its module is proportional to the mean firing rate. By taking the sensory activity originating from all the muscles of a given joint, it was demonstrated that the neurosensory sum vectors are highly correlated with the movement vectors at any point of a given trajectory (Albert et al 2005(Albert et al , 2006Bergenheim et al 2000;Jones et al 2001). Consequently, each sum vector gives the instantaneous direction and velocity of the ongoing movement (i.e., its tangential velocity).…”