Position- and scale-invariant object-centered spatial localization in monkey frontoparietal cortex dynamically adapts to cognitive demand.

Egocentric encoding is a well-known property of brain areas along the dorsal pathway. Different to previous experiments, which typically only demanded egocentric spatial processing during movement preparation, we designed a task where two male rhesus monkeys memorized an on-the-object target position and then planned a reach to this position after the object re-occurred at variable location with potentially different size. We found allocentric (in addition to egocentric) encoding in the dorsal stream reach planning areas, parietal reach region and dorsal premotor cortex, which is invariant with respect to the position, and, remarkably, also the size of the object. The dynamic adjustment from predominantly allocentric encoding during visual memory to predominantly egocentric during reach planning in the same brain areas and often the same neurons, suggests that the prevailing frame of reference is less a question of brain area or processing stream, but more of the cognitive demands.

Reward uncertainty asymmetrically affects information transmission within the monkey fronto-parietal network.

A central hypothesis in research on executive function is that controlled information processing is costly and is allocated according to the behavioral benefits it brings. However, while computational theories predict that the benefits of new information depend on prior uncertainty, the cellular effects of uncertainty on the executive network are incompletely understood. Using simultaneous recordings in monkeys, we describe several mechanisms by which the fronto-parietal network reacts to uncertainty. We show that the variance of expected rewards, independently of the value of the rewards, was encoded in single neuron and population spiking activity and local field potential (LFP) oscillations, and, importantly, asymmetrically affected fronto-parietal information transmission (measured through the coherence between spikes and LFPs). Higher uncertainty selectively enhanced information transmission from the parietal to the frontal lobe and suppressed it in the opposite direction, consistent with Bayesian principles that prioritize sensory information according to a decision maker's prior uncertainty.

Asymmetric generalization in adaptation to target displacement errors in humans and in a neural network model.

Different error signals can induce sensorimotor adaptation during visually guided reaching, possibly evoking different neural adaptation mechanisms. Here we investigate reach adaptation induced by visual target errors without perturbing the actual or sensed hand position. We analyzed the spatial generalization of adaptation to target error to compare it with other known generalization patterns and simulated our results with a neural network model trained to minimize target error independent of prediction errors. Subjects reached to different peripheral visual targets and had to adapt to a sudden fixed-amplitude displacement ("jump") consistently occurring for only one of the reach targets. Subjects simultaneously had to perform contralateral unperturbed saccades, which rendered the reach target jump unnoticeable. As a result, subjects adapted by gradually decreasing reach errors and showed negative aftereffects for the perturbed reach target. Reach errors generalized to unperturbed targets according to a translational rather than rotational generalization pattern, but locally, not globally. More importantly, reach errors generalized asymmetrically with a skewed generalization function in the direction of the target jump. Our neural network model reproduced the skewed generalization after adaptation to target jump without having been explicitly trained to produce a specific generalization pattern. Our combined psychophysical and simulation results suggest that target jump adaptation in reaching can be explained by gradual updating of spatial motor goal representations in sensorimotor association networks, independent of learning induced by a prediction-error about the hand position. The simulations make testable predictions about the underlying changes in the tuning of sensorimotor neurons during target jump adaptation.

Corrigendum: Spatial task context makes short-latency reaches prone to induced Roelofs illusion.

[This corrects the article on p. 673 in vol. 8, PMID: 25221500.].

Spatial task context makes short-latency reaches prone to induced Roelofs illusion.

The perceptual localization of an object is often more prone to illusions than an immediate visuomotor action towards that object. The induced Roelofs effect (IRE) probes the illusory influence of task-irrelevant visual contextual stimuli on the processing of task-relevant visuospatial instructions during movement preparation. In the IRE, the position of a task-irrelevant visual object induces a shift in the localization of a visual target when subjects indicate the position of the target by verbal response, key-presses or delayed pointing to the target ("perception" tasks), but not when immediately pointing or reaching towards it without instructed delay ("action" tasks). This discrepancy was taken as evidence for the dual-visual-stream or perception-action hypothesis, but was later explained by a phasic distortion of the egocentric spatial reference frame which is centered on subjective straight-ahead (SSA) and used for reach planning. Both explanations critically depend on delayed movements to explain the IRE for action tasks. Here we ask: first, if the IRE can be observed for short-latency reaches; second, if the IRE in fact depends on a distorted egocentric frame of reference. Human subjects were tested in new versions of the IRE task in which the reach goal had to be localized with respect to another object, i.e., in an allocentric reference frame. First, we found an IRE even for immediate reaches in our allocentric task, but not for an otherwise similar egocentric control task. Second, the IRE depended on the position of the task-irrelevant frame relative to the reference object, not relative to SSA. We conclude that the IRE for reaching does not mandatorily depend on prolonged response delays, nor does it depend on motor planning in an egocentric reference frame. Instead, allocentric encoding of a movement goal is sufficient to make immediate reaches susceptible to IRE, underlining the context dependence of visuomotor illusions.