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Fuglevand, A. J.

Publications and source records attributed to Fuglevand, A. J..

4 recordsLinked to original sources

Uncertainty Shapes Neural Dynamics in Motor Cortex During Reaching

Voluntary reaching movements are often made with incomplete information about the movement goal, which may require the brain to flexibly adjust motor plans and ongoing movements. To examine how uncertainty about a reach target influences neural preparation and execution, we recorded activity from dorsal premotor (PMd) and primary motor (M1) cortices of a rhesus macaque trained to reach to one of two potential targets. In the task, a timing cue flashed three times in succession. Potential targets were displayed at the time of the first flash and the monkey needed to initiate the movement almost simultaneously with the third flash. Colorings of potential targets indicated the probability that the target would be at one location or the other, thereby inducing varying levels of uncertainty about the final target location. On half the trials, the final target was displayed so late that the monkey had to guess the target location, based on cues provided by the potential targets. While the monkey performed this task, we recorded 165 neurons from PMd and 37 from M1. Population neural trajectories in the preparatory subspace of PMd (but not M1) were progressively less expansive with higher levels of uncertainty. Despite differences in preparatory states associated with uncertainty, the movements produced were the same. The narrower separation between states suggested a neural-based explanation for more rapid movement re-preparation with higher uncertainty. Furthermore, we found a dimension in neural state-space representing the level of uncertainty during movement preparation and execution. SIGNIFICANCE STATEMENTThe dorsal premotor cortex (PMd) in primates plays a critical role in organizing preparatory states needed for the execution of target-directed movements mediated downstream by the primary motor cortex (M1). But what if the location of the target is uncertain - as often occurs in our daily lives, such as reaching for a pair of glasses in the dark that have fallen to the floor. We found that different levels of uncertainty are clearly represented in population neural activity during preparation for movement in monkey PMd but not M1. Furthermore, these different neural states related to uncertainty were not associated with changes in the movements produced. These findings provide further insight (and questions) about the operations of the motor cortex.

neuroscience↗

Adaptations in common synaptic inputs to spinal motor neurons during grasping versus a less functional hand task

Previous evidence suggests that shared synaptic inputs across spinal motor neurons play a key role in coordinating multiple muscles during hand movements, reducing control complexity. In this study, we investigated how the nervous system modulates these common synaptic inputs during a functionally relevant grip (grasping) compared to less functionally relevant hand tasks. Seventeen participants performed three different tasks: simultaneous four-finger flexion without thumb involvement (four-finger flexion), thumb flexion, and simultaneous flexion of both fingers and thumb (grasping). For each task, subjects sustained isometric contractions at 5% and 15% of maximal voluntary contraction, while high-density surface electromyograms (HDsEMG) were recorded from the superficial extrinsic flexor muscles of the hand. Motor unit spike trains were decomposed from HDsEMG and tracked across tasks, and their mean discharge rate was calculated. Coherence between motor units was quantified within the delta, alpha, and beta bands to estimate common synaptic oscillations. At both force levels, the mean discharge rate decreased during grasping compared to four-finger flexion but increased during grasping compared to thumb flexion. Additionally, the area under the curve of coherence within the alpha band decreased by [~]20% during grasping compared to the four-finger flexion task, with no significant delta or beta bands changes. These reductions in alpha band coherence were reflected in force oscillations, showing decreased force-neural drive coupling within the alpha band and increased force steadiness during grasping compared to four-finger flexion. Our findings suggest that a functionally relevant and frequently used grip involves distinct neural control mechanisms that ultimately enhance force control.

neuroscience↗

Interoceptive Signals Bias Decision Making in Rhesus Macaques

Several influential theories have proposed that interoceptive signals, sent from the body to the brain, contribute to neural processes that coordinate complex behaviors. We altered the physiological state of the body using compounds that have minimal effect on the brain and evaluated their effect on decision-making in rhesus monkeys. We used glycopyrrolate, a non-specific muscarinic (parasympathetic) antagonist, and isoproterenol, a beta-1/2 (sympathetic) agonist, to create a sympathetic-dominated state in the periphery, that was indexed by increased heart rate. Rhesus monkeys were trained on two variants of an approach-avoidance conflict task. The tasks offered a choice between enduring mildly aversive stimuli in exchange for a steady flow of rewards, or cancelling the aversive stimuli, forgoing the rewards. The delay to interrupt the aversive stimuli was used as a measure of monkeys tolerance for contact with a hot but not painful stimulus or airflow directed at their muzzle. Both drugs reduced tolerance for the aversive stimuli. To determine whether the drug-induced autonomic state reduced the subjective value of the reward, we tested the effects of glycopyrrolate on a food preference task. Food preference was unaltered, suggesting that the sympathetic dominated state in the periphery selectively reduces tolerance for aversive stimuli without altering reward-seeking behaviors. As the drugs used are expected to have little or no direct effect on the brain, the observed biases in decision making are likely induced by interoceptive afferents that signal to the brain the physiological state of the body. Significance statementThe brain adjusts body physiology to the behavioral agenda of the organism through autonomic efferents; concomitantly interoceptive afferents carry signals that inform the brain about the physiological state of the body, closing a homeostatic regulatory loop. Persuasive theories proposed that interoceptive afferents contribute to higher cognitive functions, including emotion. Empirical evidence that these signals are sufficient to bias complex behavior has been limited by the difficulty of isolating interoceptive afferents from the rest of the homeostatic loop. Here we selectively manipulated the autonomic state of the body using drugs with limited penetrance of the brain in macaques performing decision-making tasks. Sympathetic-dominated peripheral states significantly altered decision making, suggesting that changes in interoceptive afferent signals are sufficient to bias behavior.

neuroscience↗

A context-dependent switch from sensing to feeling in the primate amygdala

The skin transmits affective signals that integrate into our social vocabulary. As the socio-affective aspects of touch are likely processed in the amygdala, we compared neural responses to social grooming and gentle airflow recorded from the amygdala and the primary somatosensory cortex of non-human primates. Neurons in the somatosensory cortex responded to both types of tactile stimuli. In the amygdala, however, neurons did not respond to individual grooming sweeps even though grooming elicited autonomic states indicative of positive affect. Instead, many showed changes in baseline firing rates that persisted throughout the grooming bout. Such baseline fluctuations were attributed to social context because the presence of the groomer alone could account for the observed changes in baseline activity. It appears, therefore, that during grooming, the amygdala stops responding to external inputs on a short time scale but remains responsive to social context (or the associated affective states) on longer time scales.

neuroscience↗