Paul M. Bays

Dynamic Shifts of Limited Working Memory Resources in Human Vision

Our ability to remember what we have seen is very limited. Most current views characterize this limit as a fixed number of items—only four objects—that can be held in visual working memory. We show that visual memory capacity is not fixed by the number of objects, but rather is a limited resource that is shared out dynamically between all items in the visual scene. This resource can be shifted flexibly between objects, with allocation biased by selective attention and toward targets of upcoming eye movements. The proportion of resources allocated to each item determines the precision with which it is remembered, a relation that we show is governed by a simple power law, allowing quantitative estimates of resource distribution in a scene.

Failure to Consolidate the Consolidation Theory of Learning for Sensorimotor Adaptation Tasks

An influential idea in human motor learning is that there is a consolidation period during which motor memories are transformed from a fragile to a permanent state, no longer susceptible to interference from new learning. The evidence supporting this idea comes from studies showing that the motor memory of a task (A) is lost when an opposing task (B) is experienced soon after, but not if sufficient time is allowed to pass (∼6 hr). We report results from three laboratories challenging this consolidation idea. We used an ABA paradigm in the context of a reaching task to assess the influence of experiencing B after A on the retention of A. In two experiments using visuomotor rotations, we found that B fully interferes with the retention of A even when B is experienced 24 hr after A. Contrary to previous reports, in four experiments on learning force fields, we also observed full interference between A and B when they are separated by 24 hr or even 1 week. This latter result holds for both position-dependent and velocity-dependent force fields. For both the visuomotor and force-field tasks, complete interference is still observed when the possible affects of anterograde interference are controlled through the use of washout trials. Our results fail to support the idea that motor memories become consolidated into a protected state. Rather, they are consistent with recent ideas of memory formation, which propose that memories can shift between active and inactive states.

Computational principles of sensorimotor control that minimize uncertainty and variability

Sensory and motor noise limits the precision with which we can sense the world and act upon it. Recent research has begun to reveal computational principles by which the central nervous system reduces the sensory uncertainty and movement variability arising from this internal noise. Here we review the role of optimal estimation and sensory filtering in extracting the sensory information required for motor planning, and the role of optimal control, motor adaptation and impedance control in the specification of the motor output signal.

Perception of the Consequences of Self-Action Is Temporally Tuned and Event Driven

It has been proposed that in order to increase the salience of sensations with an external cause, sensations that are predictable based on ones own actions are attenuated [1 and 2]. This may explain why self-imposed tickle [3 and 4] or constant forces [5] are perceived as less intense than the same stimuli externally imposed. Here, subjects used their right index finger to tap a force sensor mounted above their left index finger. When a motor generated a tap on the left finger synchronously with the right tap, simulating contact between the fingers, the perception of force in the left finger was attenuated compared to the same tap experienced during rest. Attenuation gradually reduced as the left tap was either delayed or advanced relative to the active right tap. However, no attenuation was seen to left taps triggered by right-finger movements that stopped above or passed wide of the sensor. We conclude that there is a window of sensory attenuation that is broadly temporally tuned and centered on the time at which the fingers would normally make contact. That is, predictive tactile sensory attenuation is linked to specific external events arising from movement rather than to the movement per se.

Dynamic Updating of Working Memory Resources for Visual Objects

Recent neurophysiological and imaging studies have investigated how neural representations underlying working memory (WM) are dynamically updated for objects presented sequentially. Although such studies implicate information encoded in oscillatory activity across distributed brain networks, interpretation of findings depends crucially on the underlying conceptual model of how memory resources are distributed. Here, we quantify the fidelity of human memory for sequences of colored stimuli of different orientation. The precision with which each orientation was recalled declined with increases in total memory load, but also depended on when in the sequence it appeared. When one item was prioritized, its recall was enhanced, but with corresponding decrements in precision for other objects. Comparison with the same number of items presented simultaneously revealed an additional performance cost for sequential display that could not be explained by temporal decay. Memory precision was lower for sequential compared with simultaneous presentation, even when each item in the sequence was presented at a different location. Importantly, stochastic modeling established this cost for sequential display was due to misbinding object features (color and orientation). These results support the view that WM resources can be dynamically and flexibly updated as new items have to be stored, but redistribution of resources with the addition of new items is associated with misbinding object features, providing important constraints and a framework for interpreting neural data.

Attenuation of self-generated tactile sensations is predictive, not postdictive.

When one finger touches the other, the resulting tactile sensation is perceived as weaker than the same stimulus externally imposed. This attenuation of sensation could result from a predictive process that subtracts the expected sensory consequences of the action, or from a postdictive process that alters the perception of sensations that are judged after the event to be self-generated. In this study we observe attenuation even when the fingers unexpectedly fail to make contact, supporting a predictive process. This predictive attenuation of self-generated sensation may have evolved to enhance the perception of sensations with an external cause.

Rapid forgetting prevented by retrospective attention cues.

Recent studies have demonstrated that memory performance can be enhanced by a cue which indicates the item most likely to be subsequently probed, even when that cue is delivered seconds after a stimulus array is extinguished. Although such retro-cuing has attracted considerable interest, the mechanisms underlying it remain unclear. Here, we tested the hypothesis that retro-cues might protect an item from degradation over time. We employed two techniques that previously have not been deployed in retro-cuing tasks. First, we used a sensitive, continuous scale for reporting the orientation of a memorized item, rather than binary measures (change or no change) typically used in previous studies. Second, to investigate the stability of memory across time, we also systematically varied the duration between the retro-cue and report. Although accuracy of reporting uncued objects rapidly declined over short intervals, retro-cued items were significantly more stable, showing negligible decline in accuracy across time and protection from forgetting. Retro-cuing an object’s color was just as advantageous as spatial retro-cues. These findings demonstrate that during maintenance, even when items are no longer visible, attention resources can be selectively redeployed to protect the accuracy with which a cued item can be recalled over time, but with a corresponding cost in recall for uncued items.

Noise in Neural Populations Accounts for Errors in Working Memory

Errors in short-term memory increase with the quantity of information stored, limiting the complexity of cognition and behavior. In visual memory, attempts to account for errors in terms of allocation of a limited pool of working memory resources have met with some success, but the biological basis for this cognitive architecture is unclear. An alternative perspective attributes recall errors to noise in tuned populations of neurons that encode stimulus features in spiking activity. I show that errors associated with decreasing signal strength in probabilistically spiking neurons reproduce the pattern of failures in human recall under increasing memory load. In particular, deviations from the normal distribution that are characteristic of working memory errors and have been attributed previously to guesses or variability in precision are shown to arise as a natural consequence of decoding populations of tuned neurons. Observers possess fine control over memory representations and prioritize accurate storage of behaviorally relevant information, at a cost to lower priority stimuli. I show that changing the input drive to neurons encoding a prioritized stimulus biases population activity in a manner that reproduces this empirical tradeoff in memory precision. In a task in which predictive cues indicate stimuli most probable for test, human observers use the cues in an optimal manner to maximize performance, within the constraints imposed by neural noise.

Spatial remapping of the visual world across saccades

Recent research has identified neurons in the visual system that remap their receptive fields before a saccade. The activity of these neurons may signal a prediction of postsaccadic visual input, derived from an efference copy of saccadic motor output. Such a prediction is often thought to underlie our perception of a stable visual world, by compensating for the shifts in retinal image that accompany each eye movement. Here we review the evidence, and conclude that prediction does not in fact play a significant role in maintaining visual stability. Instead, we consider a novel perspective in which the primary function of spatial remapping is to support three key nonperceptual processes: action control, sensorimotor adaptation and spatial memory.

Dopamine reverses reward insensitivity in apathy following globus pallidus lesions

Apathy is a complex, behavioural disorder associated with reduced spontaneous initiation of actions. Although present in mild forms in some healthy people, it is a pathological state in conditions such as Alzheimers and Parkinsons disease where it can have profoundly devastating effects. Understanding the mechanisms underlying apathy is therefore of urgent concern but this has proven difficult because widespread brain changes in neurodegenerative diseases make interpretation difficult and there is no good animal model. Here we present a very rare case with profound apathy following bilateral, focal lesions of the basal ganglia, with globus pallidus regions that connect with orbitofrontal (OFC) and ventromedial prefrontal cortex (VMPFC) particularly affected. Using two measures of oculomotor decision-making we show that apathy in this individual was associated with reward insensitivity. However, reward sensitivity could be established partially with levodopa and more effectively with a dopamine receptor agonist. Concomitantly, there was an improvement in the patients clinical state, with reduced apathy, greater motivation and increased social interactions. These findings provide a model system to study a key neuropsychiatric disorder. They demonstrate that reward insensitivity associated with basal ganglia dysfunction might be an important component of apathy that can be reversed by dopaminergic modulation.