Benjamin J. Tamber-Rosenau

Decoding cognitive control in human parietal cortex

Efficient execution of perceptual-motor tasks requires rapid voluntary reconfiguration of cognitive task sets as circumstances unfold. Such acts of cognitive control, which are thought to rely on a network of cortical regions in prefrontal and posterior parietal cortex, include voluntary shifts of attention among perceptual inputs or among memory representations, or switches between categorization or stimulus-response mapping rules. A critical unanswered question is whether task set shifts in these different domains are controlled by a common, domain-independent mechanism or by separate, domain-specific mechanisms. Recent studies have implicated a common region of medial superior parietal lobule (mSPL) as a domain-independent source of cognitive control during shifts between perceptual, mnemonic, and rule representations. Here, we use fMRI and event-related multivoxel pattern classification to show that spatial patterns of brain activity within mSPL reliably express which of several domains of cognitive control is at play on a moment-by-moment basis. Critically, these spatiotemporal brain patterns are stable over time within subjects tested several months apart and across a variety of tasks, including shifting visuospatial attention, switching categorization rules, and shifting attention in working memory.

Avoiding non-independence in fMRI data analysis: Leave one subject out

Concerns regarding certain fMRI data analysis practices have recently evoked lively debate. The principal concern regards the issue of non-independence, in which an initial statistical test is followed by further non-independent statistical tests. In this report, we propose a simple, practical solution to reduce bias in secondary tests due to non-independence using a leave-one-subject-out (LOSO) approach. We provide examples of this method, show how it reduces effect size inflation, and suggest that it can serve as a functional localizer when within-subject methods are impractical.

Cortical mechanisms of cognitive control for shifting attention in vision and working memory

Organisms operate within both a perceptual domain of objects and events, and a mnemonic domain of past experiences and future goals. Each domain requires a deliberate selection of task-relevant information, through deployments of external (perceptual) and internal (mnemonic) attention, respectively. Little is known about the control of attention shifts in working memory, or whether voluntary control of attention in these two domains is subserved by a common or by distinct functional networks. We used human fMRI to examine the neural basis of cognitive control while participants shifted attention in vision and in working memory. We found that these acts of control recruit in common a subset of the dorsal fronto-parietal attentional control network, including the medial superior parietal lobule, intraparietal sulcus, and superior frontal sulcus/gyrus. Event-related multivoxel pattern classification reveals, however, that these regions exhibit distinct spatio-temporal patterns of neural activity during internal and external shifts of attention, respectively. These findings constrain theoretical accounts of selection in working memory and perception by showing that populations of neurons in dorsal fronto-parietal network regions exhibit selective tuning for acts of cognitive control in different cognitive domains.

Amodal Processing in Human Prefrontal Cortex

Information enters the cortex via modality-specific sensory regions, whereas actions are produced by modality-specific motor regions. Intervening central stages of information processing map sensation to behavior. Humans perform this central processing in a flexible, abstract manner such that sensory information in any modality can lead to response via any motor system. Cognitive theories account for such flexible behavior by positing amodal central information processing (e.g., “central executive,” Baddeley and Hitch, 1974; “supervisory attentional system,” Norman and Shallice, 1986; “response selection bottleneck,” Pashler, 1994). However, the extent to which brain regions embodying central mechanisms of information processing are amodal remains unclear. Here we apply multivariate pattern analysis to functional magnetic resonance imaging (fMRI) data to compare response selection, a cognitive process widely believed to recruit an amodal central resource across sensory and motor modalities. We show that most frontal and parietal cortical areas known to activate across a wide variety of tasks code modality, casting doubt on the notion that these regions embody a central processor devoid of modality representation. Importantly, regions of anterior insula and dorsolateral prefrontal cortex consistently failed to code modality across four experiments. However, these areas code at least one other task dimension, process (instantiated as response selection vs response execution), ensuring that failure to find coding of modality is not driven by insensitivity of multivariate pattern analysis in these regions. We conclude that abstract encoding of information modality is primarily a property of subregions of the prefrontal cortex.

Expertise Effects in Face-Selective Areas are Robust to Clutter and Diverted Attention, but not to Competition

Expertise effects for nonface objects in face-selective brain areas may reflect stable aspects of neuronal selectivity that determine how observers perceive objects. However, bottom-up (e.g., clutter from irrelevant objects) and top-down manipulations (e.g., attentional selection) can influence activity, affecting the link between category selectivity and individual performance. We test the prediction that individual differences expressed as neural expertise effects for cars in face-selective areas are sufficiently stable to survive clutter and manipulations of attention. Additionally, behavioral work and work using event related potentials suggest that expertise effects may not survive competition; we investigate this using functional magnetic resonance imaging. Subjects varying in expertise with cars made 1-back decisions about cars, faces, and objects in displays containing one or 2 objects, with only one category attended. Univariate analyses suggest car expertise effects are robust to clutter, dampened by reducing attention to cars, but nonetheless more robust to manipulations of attention than competition. While univariate expertise effects are severely abolished by competition between cars and faces, multivariate analyses reveal new information related to car expertise. These results demonstrate that signals in face-selective areas predict expertise effects for nonface objects in a variety of conditions, although individual differences may be expressed in different dependent measures depending on task and instructions.

Central attention is serial, but midlevel and peripheral attention are parallel—A hypothesis

In this brief review, we argue that attention operates along a hierarchy from peripheral through central mechanisms. We further argue that these mechanisms are distinguished not just by their functional roles in cognition, but also by a distinction between serial mechanisms (associated with central attention) and parallel mechanisms (associated with midlevel and peripheral attention). In particular, we suggest that peripheral attentional deployments in distinct representational systems may be maintained simultaneously with little or no interference, but that the serial nature of central attention means that even tasks that largely rely on distinct representational systems will come into conflict when central attention is demanded. We go on to review both the behavioral and neural evidence for this prediction. We conclude that even though the existing evidence mostly favors our account of serial central and parallel noncentral attention, we know of no experiment that has conclusively borne out these claims. As such, this article offers a framework of attentional mechanisms that will aid in guiding future research on this topic.

Crowding in Visual Working Memory Reveals Its Spatial Resolution and the Nature of Its Representations

Spatial resolution fundamentally limits any image representation. Although this limit has been extensively investigated for perceptual representations by assessing how neighboring flankers degrade the perception of a peripheral target with visual crowding, the corresponding limit for representations held in visual working memory (VWM) is unknown. In the present study, we evoked crowding in VWM and directly compared resolution in VWM and perception. Remarkably, the spatial resolution of VWM proved to be no worse than that of perception. However, mixture modeling of errors caused by crowding revealed the qualitatively distinct nature of these representations. Perceptual crowding errors arose from both increased imprecision in target representations and substitution of flankers for targets. By contrast, VWM crowding errors arose exclusively from substitutions, which suggests that VWM transforms analog perceptual representations into discrete items. Thus, although perception and VWM share a common resolution limit, exceeding this limit reveals distinct mechanisms for perceiving images and holding them in mind.

Visual imagery of faces and cars in face-selective visual areas

Neuroimaging provides a unique tool to investigate otherwise difficult-to-access mental processes like visual imagery. Prior studies support the idea that visual imagery is a top-down reinstatement of visual perception, and it is likely that this extends to object processing. Here we use functional MRI and multi-voxel pattern analysis to ask if mental imagery of cars engages the fusiform face area, similar to what is found during perception. We test only individuals who we assumed could imagine individual car models based on their above-average perceptual abilities with cars. Our results provide evidence that cars are represented differently from common objects in face-selective visual areas, at least in those with above-average car recognition ability. Moreover, pattern classifiers trained on data acquired during imagery can decode the neural response pattern acquired during perception, suggesting that the tested object categories are represented similarly during perception and visual imagery. The results suggest that, even at high-levels of visual processing, visual imagery mirrors perception to some extent, and that face-selective areas may in part support non-face object imagery.

Functional dissociation of the inferior frontal junction from the dorsal attention network in top-down attentional control

The posterior lateral prefrontal cortex-specifically, the inferior frontal junction (IFJ)-is thought to exert a key role in the control of attention. However, the precise nature of that role remains elusive. During the voluntary deployment and maintenance of visuospatial attention, the IFJ is typically coactivated with a core dorsal network consisting of the frontal eye field and superior parietal cortex. During stimulus-driven attention, IFJ instead couples with a ventrolateral network, suggesting that IFJ plays a role in attention distinct from the dorsal network. Because IFJ rapidly switches activation patterns to accommodate conditions of goal-directed and stimulus-driven attention (Asplund CL, Todd JJ, Snyder AP, Marois R. Nat Neurosci 13: 507-512, 2010), we hypothesized that IFJs primary role is to dynamically reconfigure attention rather than to maintain attention under steady-state conditions. This hypothesis predicts that in a goal-directed visuospatial cuing paradigm IFJ would transiently deploy attention toward the cued location, whereas the dorsal attention network would maintain attentional weights during the delay between cue and target presentation. Here we tested this hypothesis with functional magnetic resonance imaging while subjects were engaged in a Posner cuing task with variable cue-target delays. Both IFJ and dorsal network regions were involved in transient processes, but sustained activity was far more evident in the dorsal network than in IFJ. These results support the account that IFJ primarily acts to shift attention whereas the dorsal network is the main locus for the maintenance of stable attentional states. NEW & NOTEWORTHY Goal-directed visuospatial attention is controlled by a dorsal fronto-parietal network and lateral prefrontal cortex. However, the relative roles of these regions in goal-directed attention are unknown. Here we present evidence for their dissociable roles in the transient reconfiguration and sustained maintenance of attentional settings: while maintenance of attentional settings is confined to the dorsal network, the configuration of these settings at the beginning of an attentional episode is a function of lateral prefrontal cortex.

High-resolution Functional Magnetic Resonance Imaging Reveals Configural Processing of Cars in Right Anterior Fusiform Face Area of Car Experts

Visual object expertise correlates with neural selectivity in the fusiform face area (FFA). Although behavioral studies suggest that visual expertise is associated with increased use of holistic and configural information, little is known about the nature of the supporting neural representations. Using high-resolution 7-T functional magnetic resonance imaging, we recorded the multivoxel activation patterns elicited by whole cars, configurally disrupted cars, and car parts in individuals with a wide range of car expertise. A probabilistic support vector machine classifier was trained to differentiate activation patterns elicited by whole car images from activation patterns elicited by misconfigured car images. The classifier was then used to classify new combined activation patterns that were created by averaging activation patterns elicited by individually presented top and bottom car parts. In line with the idea that the configuration of parts is critical to expert visual perception, car expertise was negatively associated with the probability of a combined activation pattern being classified as a whole car in the right anterior FFA, a region critical to vision for categories of expertise. Thus, just as found for faces in normal observers, the neural representation of cars in right anterior FFA is more holistic for car experts than car novices, consistent with common mechanisms of neural selectivity for faces and other objects of expertise in this area.