Gain control in the sensorimotor system

Abstract

Coordinated movement depends on constant interaction between neural circuits that produce motor output and those that report sensory consequences. Fundamental to this process are mechanisms for controlling the influence that sensory signals have on motor pathways - for example, reducing feedback gains when they are disruptive and increasing gains when advantageous. Sensory gain control comes in many forms and serves diverse purposes - in some cases sensory input is attenuated to maintain movement stability and filter out irrelevant or self-generated signals, or enhanced to facilitate salient signals for improved movement execution and adaptation. The ubiquitous presence of sensory gain control across species at multiple levels of the nervous system reflects the importance of tuning the impact that feedback information has on behavioral output.

Keywords: gain control; motor corrections; motor output; movement stability; reafference; sensorimotor adaptation; sensory feedback.

Figure 1.. Sensory gain control in the nervous system.

Sensory gain, defined broadly as the ratio between the output from and the sensory input to a given system, is subject to many forms of modulation serving diverse behavioral functions. For example, during limb movement the strength of sensory feedback is regulated at the output of sensory afferents onto spinal motor neurons and interneurons, as well as in supraspinal regions that can be many synapses downstream of peripheral afferent input. As highlighted in this review, sensory feedback from the limb can be attenuated to maintain movement stability and filter out disruptive or self-generated signals. Conversely specific feedback channels can be enhanced to facilitate online corrections within a movement as well as longer-term adaptation to changing environmental conditions or novel task demands. Ultimately, the adjustment of feedback gains is complex and time-varying, and how sensory gain is modulated depends on behavioral goals and the state of the body and the environment. Given the wide range of mechanisms and roles for sensory gain control, dysfunction can cause a diversity of sensorimotor deficits and pathologies.

Figure 2.. Differential modulation of cutaneous and proprioceptive feedback gains during wrist movement.

(a) Recording setup. Cervical spinal neuron activity was recorded while monkeys performed a wrist flexion-extension task with an instructed delay controlled by a manipulandum. (b) Task sequence. The black filled squares represent a moving cursor, the solid empty squares represent central and peripheral targets, and the gray filled square represents the peripheral cue. Red arrows illustrate either active or passive movement direction. During flexion trials, the active movement and hold epochs required a wrist flexion movement, and the passive movement involved a wrist extension (and vice-versa for extension trials). (c) Identification of first-order spinal neurons. Nerve cuff electrodes were chronically implanted on peripheral nerves of the arm: the deep branch of the radial nerve (DR, purple) and the superficial branch of the radial nerve (SR, orange). Note that DR mostly projects to extensor muscles in the forearm (proprioceptive muscle afferent). SR exclusively innervates a patch of skin on the dorsal, radial aspect of the hand (cutaneous afferent). Concurrent with nerve stimulation, the activity of spinal neurons was recorded extracellularly using single metal electrodes. (d) Example of evoked response and firing rate modulation in spinal neurons. Raster plot and peristimulus time histogram (PSTH) of two spinal neurons divided into five behavioral epochs (rows). Examples of wrist extension are shown. Colored vertical lines indicate the timing of stimulation. The peak area corresponds to the gray zone in the PSTH (the white part at the bottom of the peak represents the baseline mean firing rate preceding the stimulation pulse). The x-axis represents time in milliseconds (ms), and the y-axis represents spiking probability. The PSTH bin size is 0.5 ms. During active wrist extension the response to cutaneous afferent stimulation (SR) was attenuated (orange arrow), while the response to muscle afferent stimulation (DR) was facilitated (purple arrow). (e) Attenuation of cutaneous and facilitation of proprioceptive responses. Difference in peak area (top; spikes per stimulation above baseline) and mean firing rate (bottom; spikes per second) between rest and the four behavioral epochs, corresponding to the spinal neurons shown in (d). (*, P < 0.05; **, P < 0.01; ***, P < 0.001. Peak area: binomial test; Firing rate: Mann–Whitney U test). Note that while the modulation of mean firing rate was comparable between the two neurons, modulation of the peak response area diverges, suggesting that sensory gain modulation is specific to a given afferent input. Moreover, modulation of the response area began during the instructed delay period, suggesting a descending origin for proprioceptive and cutaneous gain control. Adapted from Confais et al. [18]••.

Figure 3.. Attenuation of auditory reafference by cortical circuits.

(a) Acoustic virtual reality behavioral setup. Head-fixed mice ran on a treadmill and heard tones whose frequency corresponded to running speed. As they acclimated to the task, mice learned an auditory reafference associated with their locomotion. (b) Association of locomotor output and auditory feedback. Black traces represent locomotion speed and red traces represent tone frequency aligned to motor output. (c) Extracellular recordings from neurons in auditory cortex reveal attenuation of reafferent auditory feedback. Left plots show population PSTH to reafferent and non-reafferent tones after acclimation to the task. y-axis shows spikes per second. During running, auditory cortical responses to reafferent tones were suppressed relative to non-reafferent tones (red traces). Right plot shows average locomotion-related suppression of auditory cortical neurons across mice. Center of plot represents the expected reafferent tone frequency. y-axis represents locomotion-related gain, defined as the ratio of the neuronal response strength during running versus rest. Suppression was greatest for the reafferent tone relative to tones of different octaves. Black bars show standard error and blue shading shows 95% confidence bounds. (d) Motor cortical modulation of reafferent auditory gains. Data from this study support a model in which secondary motor cortex (M2) recruits inhibitory neurons in auditory cortex that locally inhibit excitatory neurons. During acclimation to the task, M2 inputs onto inhibitory neurons that are tuned to the reafferent frequency are strengthened, providing a mechanism for selective gating of self-generated auditory feedback by motor cortex. Adapted from Schneider et al. [32]••.