Edward F. Ester

Stimulus-Specific Delay Activity in Human Primary Visual Cortex

Working memory (WM) involves maintaining information in an on-line state. One emerging view is that information in WM is maintained via sensory recruitment, such that information is stored via sustained activity in the sensory areas that encode the to-be-remembered information. Using functional magnetic resonance imaging, we observed that key sensory regions such as primary visual cortex (V1) showed little evidence of sustained increases in mean activation during a WM delay period, though such amplitude increases have typically been used to determine whether a region is involved in on-line maintenance. However, a multivoxel pattern analysis of delay-period activity revealed a sustained pattern of activation in V1 that represented only the intentionally stored feature of a multifeature object. Moreover, the pattern of delay activity was qualitatively similar to that observed during the discrimination of sensory stimuli, suggesting that WM representations in V1 are reasonable “copies” of those evoked during pure sensory processing.

Spatially Global Representations in Human Primary Visual Cortex during Working Memory Maintenance

Recent studies suggest that visual features are stored in working memory (WM) via sensory recruitment or sustained stimulus-specific patterns of activity in cortical regions that encode memoranda. One important question concerns the spatial extent of sensory recruitment. One possibility is that sensory recruitment is restricted to neurons that are retinotopically mapped to the positions occupied by the remembered items. Alternatively, specific feature values could be represented via a spatially global recruitment of neurons that encode the remembered feature, regardless of the retinotopic position of the remembered stimulus. Here, we evaluated these alternatives by requiring subjects to remember the orientation of a grating presented in the left or right visual field. Functional magnetic resonance imaging and multivoxel pattern analysis were then used to examine feature-specific activations in early visual regions during memory maintenance. Activation patterns that discriminated the remembered feature were found in regions of contralateral visual cortex that corresponded to the retinotopic position of the remembered item, as well as in ipsilateral regions that were not retinotopically mapped to the position of the stored stimulus. These results suggest that visual details are held in WM through a spatially global recruitment of early sensory cortex. This spatially global recruitment may enhance memory precision by facilitating robust population coding of the stored information.

A neural measure of precision in visual working memory

Recent studies suggest that the temporary storage of visual detail in working memory is mediated by sensory recruitment or sustained patterns of stimulus-specific activation within feature-selective regions of visual cortex. According to a strong version of this hypothesis, the relative “quality” of these patterns should determine the clarity of an individuals memory. Here, we provide a direct test of this claim. We used fMRI and a forward encoding model to characterize population-level orientation-selective responses in visual cortex while human participants held an oriented grating in memory. This analysis, which enables a precise quantitative description of multivoxel, population-level activity measured during working memory storage, revealed graded response profiles whose amplitudes were greatest for the remembered orientation and fell monotonically as the angular distance from this orientation increased. Moreover, interparticipant differences in the dispersion—but not the amplitude—of these response profiles were strongly correlated with performance on a concurrent memory recall task. These findings provide important new evidence linking the precision of sustained population-level responses in visual cortex and memory acuity.

Reconstructions of Information in Visual Spatial Working Memory Degrade with Memory Load

Working memory (WM) enables the maintenance and manipulation of information relevant to behavioral goals. Variability in WM ability is strongly correlated with IQ [1], and WM function is impaired in many neurological and psychiatric disorders [2, 3], suggesting that this system is a core component of higher cognition. WM storage is thought to be mediated by patterns of activity in neural populations selective for specific properties (e.g., color, orientation, location, and motion direction) of memoranda [4-13]. Accordingly, many models propose that differences in the amplitude of these population responses should be related to differences in memory performance [14, 15]. Here, we used functional magnetic resonance imaging and an image reconstruction technique based on a spatial encoding model [16] to visualize and quantify population-level memory representations supported by multivoxel patterns of activation within regions of occipital, parietal and frontal cortex while participants precisely remembered the location(s) of zero, one, or two small stimuli. We successfully reconstructed images containing representations of the remembered-but not forgotten-locations within regions of occipital, parietal, and frontal cortex using delay-period activation patterns. Critically, the amplitude of representations of remembered locations and behavioral performance both decreased with increasing memory load. These results suggest that differences in visual WM performance between memory load conditions are mediated by changes in the fidelity of large-scale population response profiles distributed across multiple areas of human cortex.

Restoring Latent Visual Working Memory Representations in Human Cortex

Working memory (WM) enables the storage and manipulation of limited amounts of information over short periods. Prominent models posit that increasing the number of remembered items decreases the spiking activity dedicated to each item via mutual inhibition, which irreparably degrades the fidelity of each items representation. We tested these models by determining if degraded memory representations could be recovered following a post-cue indicating which of several items in spatial WM would be recalled. Using an fMRI-based image reconstruction technique, we identified impaired behavioral performance and degraded mnemonic representations with elevated memory load. However, in several cortical regions, degraded mnemonic representations recovered substantially following a post-cue, and this recovery tracked behavioral performance. These results challenge pure spike-based models of WM and suggest that remembered items are additionally encoded within latent or hidden neural codes that can help reinvigorate active WM representations.

A bilateral advantage for storage in visual working memory

Various studies have demonstrated enhanced visual processing when information is presented across both visual hemifields rather than in a single hemifield (the bilateral advantage). For example, Alvarez and Cavanagh (2005) reported that observers were able to track twice as many moving visual stimuli when the tracked items were presented bilaterally rather than unilaterally, suggesting that independent resources enable tracking in the two visual fields. Motivated by similarities in the apparent capacity and neural substrates that mediate tracking and visual working memory (WM), the present work examined whether or not a bilateral advantage also arises during storage in visual WM. Using a recall procedure to assess working memory for orientation information, we found a reliable bilateral advantage; recall error was smaller with bilateral sample displays than with unilateral displays. To demonstrate that the bilateral advantage influenced storage per se rather than just encoding efficiency, we replicated the observed bilateral advantage using sequentially presented stimuli. Finally, to further characterize how bilateral presentations enhanced storage in working memory, we measured both the number and the resolution of the stored items and found that bilateral presentations lead to an increased probability of storage, rather than enhanced mnemonic resolution. Thus, the bilateral advantage extends beyond the initial selection and encoding of visual information to influence online maintenance in visual working memory.

Sensory gain outperforms efficient readout mechanisms in predicting attention-related improvements in behavior.

Spatial attention has been postulated to facilitate perceptual processing via several different mechanisms. For instance, attention can amplify neural responses in sensory areas (sensory gain), mediate neural variability (noise modulation), or alter the manner in which sensory signals are selectively read out by postsensory decision mechanisms (efficient readout). Even in the context of simple behavioral tasks, it is unclear how well each of these mechanisms can account for the relationship between attention-modulated changes in behavior and neural activity because few studies have systematically mapped changes between stimulus intensity, attentional focus, neural activity, and behavioral performance. Here, we used a combination of psychophysics, event-related potentials (ERPs), and quantitative modeling to explicitly link attention-related changes in perceptual sensitivity with changes in the ERP amplitudes recorded from human observers. Spatial attention led to a multiplicative increase in the amplitude of an early sensory ERP component (the P1, peaking ∼80–130 ms poststimulus) and in the amplitude of the late positive deflection component (peaking ∼230–330 ms poststimulus). A simple model based on signal detection theory demonstrates that these multiplicative gain changes were sufficient to account for attention-related improvements in perceptual sensitivity, without a need to invoke noise modulation. Moreover, combining the observed multiplicative gain with a postsensory readout mechanism resulted in a significantly poorer description of the observed behavioral data. We conclude that, at least in the context of relatively simple visual discrimination tasks, spatial attention modulates perceptual sensitivity primarily by modulating the gain of neural responses during early sensory processing

Visual crowding cannot be wholly explained by feature pooling.

Visual perception is dramatically impaired when a peripheral target is embedded within clutter, a phenomenon known as visual crowding. Despite decades of study, the mechanisms underlying crowding remain a matter of debate. Feature pooling models assert that crowding results from a compulsory pooling (e.g., averaging) of target and distractor features. This view has been extraordinarily influential in recent years, so much so that crowding is typically regarded as synonymous with pooling. However, many demonstrations of feature pooling can also be accommodated by a probabilistic substitution model where observers occasionally report a distractor as the target. Here, we directly compared pooling and substitution using an analytical approach sensitive to both alternatives. In four experiments, we asked observers to report the precise orientation of a target stimulus flanked by two irrelevant distractors. In all cases, the observed data were well described by a quantitative model that assumes probabilistic substitution, and poorly described by a quantitative model that assumes that targets and distractors are averaged. These results challenge the widely held assumption that crowding can be wholly explained by compulsory pooling.

Feature-selective attentional modulations in human frontoparietal cortex

Control over visual selection has long been framed in terms of a dichotomy between “source” and “site,” where top-down feedback signals originating in frontoparietal cortical areas modulate or bias sensory processing in posterior visual areas. This distinction is motivated in part by observations that frontoparietal cortical areas encode task-level variables (e.g., what stimulus is currently relevant or what motor outputs are appropriate), while posterior sensory areas encode continuous or analog feature representations. Here, we present evidence that challenges this distinction. We used fMRI, a roving searchlight analysis, and an inverted encoding model to examine representations of an elementary feature property (orientation) across the entire human cortical sheet while participants attended either the orientation or luminance of a peripheral grating. Orientation-selective representations were present in a multitude of visual, parietal, and prefrontal cortical areas, including portions of the medial occipital cortex, the lateral parietal cortex, and the superior precentral sulcus (thought to contain the human homolog of the macaque frontal eye fields). Additionally, representations in many—but not all—of these regions were stronger when participants were instructed to attend orientation relative to luminance. Collectively, these findings challenge models that posit a strict segregation between sources and sites of attentional control on the basis of representational properties by demonstrating that simple feature values are encoded by cortical regions throughout the visual processing hierarchy, and that representations in many of these areas are modulated by attention. SIGNIFICANCE STATEMENT Influential models of visual attention posit a distinction between top-down control and bottom-up sensory processing networks. These models are motivated in part by demonstrations showing that frontoparietal cortical areas associated with top-down control represent abstract or categorical stimulus information, while visual areas encode parametric feature information. Here, we show that multivariate activity in human visual, parietal, and frontal cortical areas encode representations of a simple feature property (orientation). Moreover, representations in several (though not all) of these areas were modulated by feature-based attention in a similar fashion. These results provide an important challenge to models that posit dissociable top-down control and sensory processing networks on the basis of representational properties.

Attending Multiple Items Decreases the Selectivity of Population Responses in Human Primary Visual Cortex

Multiple studies have documented an inverse relationship between the number of to-be-attended or remembered items in a display (“set size”) and task performance. The neural source of this decline in cognitive performance is currently under debate. Here, we used a combination of fMRI and a forward encoding model of orientation selectivity to generate population tuning functions for each of two stimuli while human observers attended either one or both items. We observed (1) clear population tuning functions for the attended item(s) that peaked at the stimulus orientation and decreased monotonically as the angular distance from this orientation increased, (2) a set-size-dependent decline in the relative precision of orientation-specific population responses, such that attending two items yielded a decline in selectivity of the population tuning function for each item, and (3) that the magnitude of the loss of precision in population tuning functions predicted individual differences in the behavioral cost of attending an additional item. These findings demonstrate that attending multiple items degrades the precision of perceptual representations for the target items and provides a straightforward account for the associated impairments in visually guided behavior.