The critical stability task: quantifying sensory-motor control during ongoing movement in nonhuman primates

Everyday behaviors require that we interact with the environment, using sensory information in an ongoing manner to guide our actions. Yet, by design, many of the tasks used in primate neurophysiology laboratories can be performed with limited sensory guidance. As a consequence, our knowledge about the neural mechanisms of motor control is largely limited to the feedforward aspects of the motor command. To study the feedback aspects of volitional motor control, we adapted the critical stability task (CST) from the human performance literature (Jex H, McDonnell J, Phatak A. IEEE Trans Hum Factors Electron 7: 138–145, 1966). In the CST, our monkey subjects interact with an inherently unstable (i.e., divergent) virtual system and must generate sensory-guided actions to stabilize it about an equilibrium point. The difficulty of the CST is determined by a single parameter, which allows us to quantitatively establish the limits of performance in the task for different sensory feedback conditions. Two monkeys learned to perform the CST with visual or vibrotactile feedback. Performance was better under visual feedback, as expected, but both monkeys were able to utilize vibrotactile feedback alone to successfully perform the CST. We also observed changes in behavioral strategy as the task became more challenging. The CST will have value for basic science investigations of the neural basis of sensory-motor integration during ongoing actions, and it may also provide value for the design and testing of bidirectional brain computer interface systems. NEW & NOTEWORTHY Currently, most behavioral tasks used in motor neurophysiology studies require primates to make short-duration, stereotyped movements that do not necessitate sensory feedback. To improve our understanding of sensorimotor integration, and to engineer meaningful artificial sensory feedback systems for brain-computer interfaces, it is crucial to have a task that requires sensory feedback for good control. The critical stability task demands that sensory information be used to guide long-duration movements.

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The emulation theory of representation: Motor control, imagery, and perception

Behavioral and Brain Sciences ◽

10.1017/s0140525x04000093 ◽

2004 ◽

Vol 27 (3) ◽

pp. 377-396 ◽

Cited By ~ 565

Author(s):

Rick Grush

Keyword(s):

Motor Control ◽

Sensory Feedback ◽

Sensory Input ◽

Neural Circuits ◽

Sensory Information ◽

The Body ◽

Feedback Delay ◽

Run Off ◽

Effects Of Feedback ◽

The Brain

The emulation theory of representation is developed and explored as a framework that can revealingly synthesize a wide variety of representational functions of the brain. The framework is based on constructs from control theory (forward models) and signal processing (Kalman filters). The idea is that in addition to simply engaging with the body and environment, the brain constructs neural circuits that act as models of the body and environment. During overt sensorimotor engagement, these models are driven by efference copies in parallel with the body and environment, in order to provide expectations of the sensory feedback, and to enhance and process sensory information. These models can also be run off-line in order to produce imagery, estimate outcomes of different actions, and evaluate and develop motor plans. The framework is initially developed within the context of motor control, where it has been shown that inner models running in parallel with the body can reduce the effects of feedback delay problems. The same mechanisms can account for motor imagery as the off-line driving of the emulator via efference copies. The framework is extended to account for visual imagery as the off-line driving of an emulator of the motor-visual loop. I also show how such systems can provide for amodal spatial imagery. Perception, including visual perception, results from such models being used to form expectations of, and to interpret, sensory input. I close by briefly outlining other cognitive functions that might also be synthesized within this framework, including reasoning, theory of mind phenomena, and language.

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Advantages of comparative studies in songbirds to understand the neural basis of sensorimotor integration

Journal of Neurophysiology ◽

10.1152/jn.00623.2016 ◽

2017 ◽

Vol 118 (2) ◽

pp. 800-816 ◽

Cited By ~ 17

Author(s):

Karagh Murphy ◽

Logan S. James ◽

Jon T. Sakata ◽

Jonathan F. Prather

Keyword(s):

Nervous System ◽

Sensory Feedback ◽

Sensorimotor Integration ◽

New Technologies ◽

Sensory Information ◽

Neural Basis ◽

Communication Behaviors ◽

Song Repertoire ◽

Evolutionary Variation ◽

And Control

Sensorimotor integration is the process through which the nervous system creates a link between motor commands and associated sensory feedback. This process allows for the acquisition and refinement of many behaviors, including learned communication behaviors such as speech and birdsong. Consequently, it is important to understand fundamental mechanisms of sensorimotor integration, and comparative analyses of this process can provide vital insight. Songbirds offer a powerful comparative model system to study how the nervous system links motor and sensory information for learning and control. This is because the acquisition, maintenance, and control of birdsong critically depend on sensory feedback. Furthermore, there is an incredible diversity of song organizations across songbird species, ranging from songs with simple, stereotyped sequences to songs with complex sequencing of vocal gestures, as well as a wide diversity of song repertoire sizes. Despite this diversity, the neural circuitry for song learning, control, and maintenance remains highly similar across species. Here, we highlight the utility of songbirds for the analysis of sensorimotor integration and the insights about mechanisms of sensorimotor integration gained by comparing different songbird species. Key conclusions from this comparative analysis are that variation in song sequence complexity seems to covary with the strength of feedback signals in sensorimotor circuits and that sensorimotor circuits contain distinct representations of elements in the vocal repertoire, possibly enabling evolutionary variation in repertoire sizes. We conclude our review by highlighting important areas of research that could benefit from increased comparative focus, with particular emphasis on the integration of new technologies.

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Multimodal and Motor Influences on Orientation: Implications for Adapting to Weightless and Virtual Environments1

Journal of Vestibular Research ◽

10.3233/ves-1992-2405 ◽

1992 ◽

Vol 2 (4) ◽

pp. 307-322

Author(s):

James R. Lackner

Keyword(s):

Virtual Environments ◽

Motion Sickness ◽

Sensory Feedback ◽

Spatial Information ◽

Body Movement ◽

Sensory Information ◽

The Body ◽

Space Travel ◽

Sensory Motor ◽

Motor Information

Human sensory-motor control and orientation involve the correlation of sensory information from many modalities with motor information about ongoing patterns of voluntary and reflexive activation of the body musculature. The vestibular system represents only one of the acceleration-sensitive receptor systems of the body conveying spatial information. Touch- and pressure-dependent receptors, somatosensory and interoceptive, as well as proprioceptive receptors contribute, along with visual and auditory signals specifying relative motion between self and surround. Control of body movement and orientation is dynamically adapted to the 1G force background of Earth. Exposure to non-1G environments such as in space travel produces a variety of sensory-motor disturbances, and often motion sickness, until adaptation is achieved. Exposure to virtual environments in which body movements are not accompanied by normal patterns of inertial and sensory feedback can also lead to control errors and elicit motion sickness.

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Fast sensory–motor reactions in echolocating bats to sudden changes during the final buzz and prey intercept

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1424457112 ◽

2015 ◽

Vol 112 (13) ◽

pp. 4122-4127 ◽

Cited By ~ 17

Author(s):

Cornelia Geberl ◽

Signe Brinkløv ◽

Lutz Wiegrebe ◽

Annemarie Surlykke

Keyword(s):

Motor Control ◽

Sensory Feedback ◽

Prey Capture ◽

Emission Rates ◽

Ultrasonic Signals ◽

Acoustic Feedback ◽

Sensory Motor ◽

Air Capture ◽

High Emission ◽

Myotis Daubentonii

Echolocation is an active sense enabling bats and toothed whales to orient in darkness through echo returns from their ultrasonic signals. Immediately before prey capture, both bats and whales emit a buzz with such high emission rates (≥180 Hz) and overall duration so short that its functional significance remains an enigma. To investigate sensory–motor control during the buzz of the insectivorous bat Myotis daubentonii, we removed prey, suspended in air or on water, before expected capture. The bats responded by shortening their echolocation buzz gradually; the earlier prey was removed down to approximately 100 ms (30 cm) before expected capture, after which the full buzz sequence was emitted both in air and over water. Bats trawling over water also performed the full capture behavior, but in-air capture motions were aborted, even at very late prey removals (<20 ms = 6 cm before expected contact). Thus, neither the buzz nor capture movements are stereotypical, but dynamically adapted based on sensory feedback. The results indicate that echolocation is controlled mainly by acoustic feedback, whereas capture movements are adjusted according to both acoustic and somatosensory feedback, suggesting separate (but coordinated) central motor control of the two behaviors based on multimodal input. Bat echolocation, especially the terminal buzz, provides a unique window to extremely fast decision processes in response to sensory feedback and modulation through attention in a naturally behaving animal.

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Increasing viscosity helps explain locomotor control in swimming Polypterus seneglus

Integrative Organismal Biology ◽

10.1093/iob/obab024 ◽

2021 ◽

Author(s):

K Lutek ◽

E M Standen

Keyword(s):

Motor Control ◽

Sensory Feedback ◽

Muscle Activation ◽

Central Pattern Generators ◽

Sensory Information ◽

High Viscosity ◽

Control Input ◽

Polypterus Senegalus ◽

Similar Motor ◽

Pattern Generators

Abstract Locomotion relies on the successful integration of sensory information to adjust brain commands and basic motor rhythms created by central pattern generators. It is not clearly understood how altering the sensory environment impacts control of locomotion. In an aquatic environment, mechanical sensory feedback to the animal can be readily altered by adjusting water viscosity. Computer modeling of fish swimming systems show that, without sensory feedback, high viscosity systems dampen kinematic output despite similar motor control input. We recorded muscle activity and kinematics of six Polypterus senegalus in four different viscosities of water from 1 cP (normal water) to 40 cP. In high viscosity, P. senegalus exhibit increased body curvature, body wavespeed and body and pectoral fin frequency during swimming. These changes are the result of increased muscle activation intensity and maintain voluntary swimming speed. Unlike the sensory deprived model, intact sensory feedback allows fish to adjust swimming motor control and kinematic output in high viscous water but maintain typical swimming coordination.

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Tactile suppression stems from sensation-specific sensorimotor predictions

10.1101/2021.07.04.451060 ◽

2021 ◽

Author(s):

Elena Fuehrer ◽

Dimitris Voudouris ◽

Alexandra Lezkan ◽

Knut Drewing ◽

Katja Fiehler

Keyword(s):

Sensory Feedback ◽

Sensory Information ◽

Motor Command ◽

The Body ◽

Textured Surfaces ◽

Vibrotactile Feedback ◽

The World ◽

Tactile Sensations ◽

Predictive Mechanisms

The ability to sample sensory information with our hands is crucial for smooth and efficient interactions with the world. Despite this important role of touch, tactile sensations on a moving hand are perceived weaker than when presented on the same but stationary hand.1-3 This phenomenon of tactile suppression has been explained by predictive mechanisms, such as forward models, that estimate future sensory states of the body on the basis of the motor command and suppress the associated predicted sensory feedback.4 The origins of tactile suppression have sparked a lot of debate, with contemporary accounts claiming that suppression is independent of predictive mechanisms and is instead akin to unspecific gating.5 Here, we target this debate and provide evidence for sensation-specific tactile suppression due to sensorimotor predictions. Participants stroked with their finger over textured surfaces that caused predictable vibrotactile feedback signals on that finger. Shortly before touching the texture, we applied external vibrotactile probes on the moving finger that either matched or mismatched the frequency generated by the stroking movement. We found stronger suppression of the probes that matched the predicted sensory feedback. These results show that tactile suppression is not limited to unspecific gating but is specifically tuned to the predicted sensory states of a movement.

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