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Wolff, M. J.

Publications and source records attributed to Wolff, M. J..

8 recordsLinked to original sources

Converting color memory toward a spatial format to benefit behavior

Visual working memory allows for the brief maintenance of information to serve behavioral goals. It has been shown that when the specific action required to serve a future goal is predictable, people can flexibly change a visual memory representation to incorporate an action-based one, demonstrating the goal-oriented nature of visual working memory. Can such flexibility also be observed within the visual domain, between color and space? In this eye-tracking study, participants remembered either a centrally presented color or a spatial position around fixation. Critically, when remembering a color the response wheel was either randomly rotated, or shown at a fixed rotation, on every trial. When fixed, every target color could be associated with a predictable position on the wheel during response. Do people incorporate this added spatial information in their behavior? Participants utilized color-space associations when remembering color: Response initiation happened faster when the color wheel was fixed compared to random, irrespective of whether an action could be planned or not. Next, we showed that gaze was biased towards the position of the spatial memory target during the delay, extending previous work on gaze biases. Importantly, also when remembering a color, gaze was biased towards the anticipated position of that color on the response wheel when it was fixed. Together, our results show a behavioral benefit of added spatial information for color memory, and systematic changes in gaze that reflect flexible utilization of space.

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Visual representations in the human brain rely on a reference frame that is in between allocentric and retinocentric coordinates

Visual information in our everyday environment is anchored to an allocentric reference frame - a tall building remains upright even when you tilt your head, which changes the projection of the building on your retina from a vertical to a diagonal orientation. Does retinotopic cortex represent visual information in an allocentric or retinocentric reference frame? Here, we investigate which reference frame the brain uses by dissociating allocentric and retinocentric reference frames via a head tilt manipulation combined with electroencephalography (EEG). Nineteen participants completed between 1728-2880 trials during which they briefly viewed (150 ms) and then remembered (1500 ms) a randomly oriented target grating. In interleaved blocks of trials, the participants head was either kept upright, or tilted by 45{o} using a custom rotating chinrest. The target orientation could be decoded throughout the trial (using both voltage and alpha-band signals) when training and testing within head-upright blocks, and within head-tilted blocks. Importantly, we directly addressed the question of reference frames via cross-generalized decoding: If target orientations are represented in a retinocentric reference frame, a decoder trained on head-upright trials would predict a 45{o} offset in decoded orientation when tested on head-tilted trials (after all, a vertical building becomes diagonal on the retina after head tilt). Conversely, if target representations are allocentric and anchored to the real world, no such offset should be observed. Our analyses reveal that from the earliest stages of perceptual processing all the way throughout the delay, orientations are represented in between an allocentric and retinocentric reference frame. These results align with previous findings from physiology studies in non-human primates, and are the first to demonstrate that the human brain does not rely on a purely allocentric or retinocentric reference frame when representing visual information.

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Variable processing shifts during perceptual acceleration: Evidence from temporal integration

The perception of a stimulus can be accelerated by another that precedes it. Perceptual acceleration has been observed in a range of tasks, at varying timescales, and arises by virtue of providing advance spatial and/or temporal information about upcoming stimuli. Here we examined perceptual acceleration during visual temporal integration. Temporal integration occurs when successive stimuli appear that fit together in time as well as space. As such, stimuli arriving first during temporal integration partially predict those that follow. Although temporal integration is a rapid process, we reasoned that this information may cause perceptual acceleration during temporal integration. We used multivariate pattern analysis of EEG data from a missing element task, designed to measure the visual temporal integration of two successive stimulus displays, so that we were able to precisely track the representation associated with the integrated percept in time. We manipulated the delay between our displays, and observed commensurate acceleration of the resultant integrated representation. The degree of acceleration first increased from early (100 ms after stimulus onset) to intermediate (200 ms) processing stages, before decreasing again at a later stage (400 ms). The results thus suggest that perceptual acceleration occurs during temporal integration, but is nonlinear, such that some time that is gained at one moment in the process can be lost again at another.

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Model mimicry limits conclusions about neural tuning and can mistakenly imply unlikely priors

In a recent issue of Nature Communications, Harrison, Bays, and Rideaux1 use electroencephalography (EEG) to infer population tuning properties from human visual cortex, and deliver a major update to existing knowledge about the most elemental building block of visual perception - orientation tuning. Using EEG together with simulations in an approach they refer to as "generative forward modeling", the authors adjudicate between two competing population tuning schemes for orientation tuning in visual cortex. They claim that a redistribution of orientation tuning curves can explain their observed pattern of EEG results, and that this tuning scheme embeds a prior of natural image statistics that exhibits a previously undiscovered anisotropy between vertical and horizontal orientations. If correct, this approach could become widely used to find unique neural coding solutions to population response data (e.g., from EEG) and to yield a "true" population tuning scheme deemed generalizable to other instances. However, here we identify major flaws that invalidate the promise of this approach, which we argue should not be used at all. First, we will examine the premise of Harrison and colleagues1, to subsequently explain why "generative forward modeling" cannot circumvent model mimicry pitfalls and can deliver many possible solutions of unknowable correctness. Finally, we show a tentative alternative explanation for the data. Conflict of interestThe authors declare no conflict of interest

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Behaviorally irrelevant feature matching increases neural and behavioral working memory readout: Support for activity-silent working memory

There is an ongoing debate about whether working memory (WM) maintenance relies on persistent activity and/or short-term synaptic plasticity. This is a challenging question, because neuroimaging techniques in cognitive neuroscience measure activity only. Recently, neural perturbation techniques have been developed to tackle this issue, such as visual impulse perturbation or "pinging", which reveals (un)attended WM content during maintenance. There are contrasting explanations of how pinging reveals WM content, which is central to the debate. Pinging could reveal mnemonic representations by perturbing content-specific networks or by increasing the neural signal-to-noise ratio of active neural states. Here we tested the extent to which the neural impulse response is patterned by the WM network, by presenting two different impulse stimuli. If the impulse interacts with WM networks, the WM-specific impulse response should be enhanced by physical overlap between the initial memory item and the subsequent external perturbation stimulus. This prediction was tested in a working memory task by matching or mismatching task-irrelevant spatial frequencies between memory items and impulse stimuli, as well as probes. Matching probe spatial frequency with memory items resulted in faster behavioral response times and matching impulse spatial frequency with memory items increased the specificity of the neural impulse response as measured from EEG. Matching spatial frequencies did neither result in globally stronger neural responses nor in a larger decrease in trial-to-trial variability compared to mismatching spatial frequencies. The improved neural and behavioural readout of irrelevant feature matching provide evidence that impulse perturbation interacts directly with the memory representations.

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A gradual transition from veridical to categorical representations along the visual hierarchy during working memory, but not perception.

The ability to stably maintain visual information over brief delays is central to healthy cognitive functioning, as is the ability to differentiate such internal representations from external inputs. One possible way to achieve both is via multiple concurrent mnemonic representations along the visual hierarchy that differ systematically from the representations of perceptual inputs. To test this possibility, we examine orientation representations along the visual hierarchy during perception and working memory. Human participants directly viewed, or held in mind, oriented grating patterns, and the similarity between fMRI activation patterns for different orientations was calculated throughout retinotopic cortex. During direct viewing of grating stimuli, similarity was relatively evenly distributed amongst all orientations, while during working memory the similarity was higher around oblique orientations. We modeled these differences in representational geometry based on the known distribution of orientation information in the natural world: The "veridical" model uses an efficient coding framework to capture hypothesized representations during visual perception. The "categorical" model assumes that different "psychological distances" between orientations result in orientation categorization relative to cardinal axes. During direct perception, the veridical model explained the data well. During working memory, the categorical model gradually gained explanatory power over the veridical model for increasingly anterior retinotopic regions. Thus, directly viewed images are represented veridically, but once visual information is no longer tethered to the sensory world there is a gradual progression to more categorical mnemonic formats along the visual hierarchy.

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Drifting codes within a stable coding scheme for working memory

Working memory (WM) is important to maintain information over short time periods to provide some stability in a constantly changing environment. However, brain activity is inherently dynamic, raising a challenge for maintaining stable mental states. To investigate the relationship between WM stability and neural dynamics, we used electroencephalography to measure the neural response to impulse stimuli during a WM delay. Multivariate pattern analysis revealed representations were both stable and dynamic: there was a clear difference in neural states between time-specific impulse responses, reflecting dynamic changes, yet the coding scheme for memorized orientations was stable. This suggests that a stable subcomponent in WM enables stable maintenance within a dynamic system. A stable coding scheme simplifies readout for WM-guided behaviour, whereas the low-dimensional dynamic component could provide additional temporal information. Despite having a stable subspace, WM is clearly not perfect - memory performance still degrades over time. Indeed, we find that even within the stable coding scheme, memories drift during maintenance. When averaged across trials, such drift contributes to the width of the error distribution.

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Impulse responses reveal unimodal and bimodal access to visual and auditory working memory

It is unclear to what extent sensory processing areas are involved in the maintenance of sensory information in working memory (WM). Previous studies have thus far relied on finding neural activity in the corresponding sensory cortices, neglecting potential activity-silent mechanisms such as connectivity-dependent encoding. It has recently been found that visual stimulation during visual WM maintenance reveals WM-dependent changes through a bottom-up neural response. Here, we test whether this impulse response is uniquely visual and sensory-specific. Human participants (both sexes) completed visual and auditory WM tasks while electroencephalography was recorded. During the maintenance period, the WM network was perturbed serially with fixed and task-neutral auditory and visual stimuli. We show that a neutral auditory impulse-stimulus presented during the maintenance of a pure tone resulted in a WM-dependent neural response, providing evidence for the auditory counterpart to the visual WM findings reported previously. Interestingly, visual stimulation also resulted in an auditory WM-dependent impulse response, implicating the visual cortex in the maintenance of auditory information, either directly, or indirectly as a pathway to the neural auditory WM representations elsewhere. In contrast, during visual WM maintenance only the impulse response to visual stimulation was content-specific, suggesting that visual information is maintained in a sensory-specific neural network, separated from auditory processing areas.\n\nSignificance StatementWorking memory is a crucial component of intelligent, adaptive behaviour. Our understanding of the neural mechanisms that support it has recently shifted: rather than being dependent on an unbroken chain of neural activity, working memory may rely on transient changes in neuronal connectivity, which can be maintained efficiently in activity-silent brain states. Previous work using a visual impulse stimulus to perturb the memory network has implicated such silent states in the retention of line orientations in visual working memory. Here, we show that auditory working memory similarly retains auditory information. We also observed a sensory-specific impulse response in visual working memory, while auditory memory responded bi-modally to both visual and auditory impulses, possibly reflecting visual dominance of working memory.

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