Britten, K. H. | bioRxiv Science

bioRxiv2024

Context-dependence of deterministic and nondeterministic contributions to closed-loop steering control

In natural circumstances, sensory systems operate in a closed loop with motor output, whereby actions shape subsequent sensory experiences. A prime example of this is the sensorimotor processing required to align ones direction of travel, or heading, with ones goal, a behavior we refer to as steering. In steering, motor outputs work to eliminate errors between the direction of heading and the goal, modifying subsequent errors in the process. The closed-loop nature of the behavior makes it challenging to determine how deterministic and nondeterministic processes contribute to behavior. We overcome this by applying a nonparametric, linear kernel-based analysis to behavioral data of monkeys steering through a virtual environment in two experimental contexts. In a given context, the results were consistent with previous work that described the transformation as a second-order linear system. Classically, the parameters of such second-order models are associated with physical properties of the limb such as viscosity and stiffness that are commonly assumed to be approximately constant. By contrast, we found that the fit kernels differed strongly across tasks in these and other parameters, suggesting context-dependent changes in neural and biomechanical processes. We additionally fit residuals to a simple noise model and found that the form of the noise was highly conserved across both contexts and animals. Strikingly, the fitted noise also closely matched that found previously in a human steering task. Altogether, this work presents a kernel-based analysis that characterizes the context-dependence of deterministic and non-deterministic components of a closed-loop sensorimotor task. New and noteworthyWe use nonparametric systems identification techniques to assess the context-dependence of deterministic and nondeterministic contributions to a closed-loop behavior. Classical approaches assume a fixed transformation between sensory input and motor output. Here, we reveal strong changes to the measured sensorimotor transformations with behavioral context. In contrast, noise within the transformation exhibited a consistent form across contexts, subjects, and species. Together, this work demonstrates how context affects the systematic and stochastic components of a closed-loop behavior.

neuroscience↗

bioRxiv2019

Retinal stabilization reveals limited influence of extraretinal signals on heading tuning in the medial superior temporal area

Heading perception in primates depends heavily on visual optic-flow cues. Yet during self-motion, heading percepts remain stable even though smooth-pursuit eye movements often distort optic flow. Electrophysiological studies have identified visual areas in monkey cortex, including the dorsal medial superior temporal area (MSTd), that signal the true heading direction during pursuit. According to theoretical work, self-motion can be represented accurately by compensating for these distortions in two ways: via retinal mechanisms or via extraretinal efference-copy signals, which predict the sensory consequences of movement. Psychophysical evidence strongly supports the efference-copy hypothesis, but physiological evidence remains inconclusive. Neurons that signal the true heading direction during pursuit are found in visual areas of monkey cortex, including the dorsal medial superior temporal area (MSTd). Here we measured heading tuning in MSTd using a novel stimulus paradigm, in which we stabilize the optic-flow stimulus on the retina during pursuit. This approach isolates the effects on neuronal heading preferences of extraretinal signals, which remain active while the retinal stimulus is prevented from changing. Our results demonstrate a significant but small influence of extraretinal signals on the preferred heading directions of MSTd neurons. Under our stimulus conditions, which are rich in retinal cues, we find that retinal mechanisms dominate physiological corrections for pursuit eye movements, suggesting that extraretinal cues, such as predictive efference-copy mechanisms, have a limited role under naturalistic conditions.\n\nSignificance StatementSensory systems discount stimulation caused by the animals own behavior. For example, eye movements cause irrelevant retinal signals that could interfere with motion perception. The visual system compensates for such self-generated motion, but how this happens is unclear. Two theoretical possibilities are a purely visual calculation or one using an internal signal of eye movements to compensate for their effects. Such a signal can be isolated by experimentally stabilizing the image on a moving retina, but this approach has never been adopted to study motion physiology. Using this method, we find that eye-movement signals have little influence on neural activity in visual cortex, while feed-forward visual calculation has a strong effect and is likely important under real-world conditions.

neuroscience↗