Michael Esterman

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.

Control of Spatial and Feature-Based Attention in Frontoparietal Cortex

Visual attention selects task-relevant information from scenes to help achieve behavioral goals. Attention can be deployed within multiple domains to select specific spatial locations, features, or objects. Recent evidence has shown that voluntary shifts of attention in multiple domains are consistently associated with transient increases in cortical activity in medial superior parietal lobule, suggesting that this may be the source of a domain-independent control signal that initiates the reconfiguration of attention. To investigate this hypothesis, we used fMRI to measure changes in cortical activation while human subjects shifted attention between spatial locations or between colors at a location. Univariate multiple regression analysis revealed a common, domain-independent transient signal [in posterior parietal cortex (PPC) and prefrontal cortex] time-locked to shifts of attention in both domains. However, multivariate pattern classification conducted on the cortical surface revealed that the spatiotemporal pattern of activity within PPC differed reliably for spatial and feature-based attention shifts. These results suggest that the posterior parietal cortex is a common hub for the control of attention shifts but contains subpopulations of neurons with domain-specific tuning for cognitive control.

Coming Unbound: Disrupting Automatic Integration of Synesthetic Color and Graphemes by Transcranial Magnetic Stimulation of the Right Parietal Lobe

In some individuals, a visually presented letter or number automatically evokes the perception of a specific color, an experience known as color-grapheme synesthesia. It has been suggested that parietal binding mechanisms play a role in the phenomenon. We used a noninvasive stimulation technique, transcranial magnetic stimulation (TMS), to determine whether the posterior parietal lobe is critical for the integration of color and shape in color-grapheme synesthesia, as it appears to be for normal color-shape binding. Using a color-naming task with colored letters that were either congruent or incongruent with the synesthetic photism, we demonstrate that inhibition of the right posterior parietal lobe with repetitive TMS transiently attenuates synesthetic binding. These findings suggest that synesthesia (the induction of color from shape) relies on similar mechanisms as found in normal perception (where the perception of color is induced by wavelength).

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.

Different Effects of Voluntary and Involuntary Attention on EEG Activity in the Gamma Band

Previous studies have shown that EEG activity in the gamma range can be modulated by attention. Here, we compared this activity for voluntary and involuntary spatial attention in a spatial-cueing paradigm with faces as targets. The stimuli and trial timing were kept constant across attention conditions with only the predictive value of the cue changing. Gamma-band response was linked to voluntary shifts of attention, but not to the involuntary capture of attention. The presence of increased gamma responses for the voluntary allocation of attention, and its absence in cases of involuntary capture suggests that the neural mechanisms governing these two types of attention are different. Moreover, these data allow a description of the temporal dynamics contributing to the dissociation between voluntary and involuntary attention. The distribution of this correlate of voluntary attention is consistent with a top-down process involving contralateral anterior and posterior regions.

Intrinsic Fluctuations in Sustained Attention and Distractor Processing

Although sustaining a moderate level of attention is critical in daily life, evidence suggests that attention is not deployed consistently, but rather fluctuates from moment to moment between optimal and suboptimal states. To better characterize these states in humans, the present study uses a gradual-onset continuous performance task with irrelevant background distractors to explore the relationship among behavioral fluctuations, brain activity, and, in particular, the processing of visual distractors. Using fMRI, we found that reaction time variability, a continuous measure of attentional instability, was positively correlated with activity in task-positive networks and negatively correlated with activity in the task-negative default mode network. We also observed greater processing of distractor images during more stable and less error prone “in the zone” epochs compared with suboptimal “out of the zone” epochs of the task. Overall, the data suggest that optimal states of attention are accomplished with more efficient and potentially less effortful recruitment of task-relevant resources, freeing remaining resources to process task irrelevant features of the environment.

Preattentive and Attentive Visual Search in Individuals With Hemispatial Neglect

Preattentive and attentive visual processing was examined in patients with hemispatial neglect, hemispatial neglect with hemianopia, and control participants. In the preattentive search task, targets possessed a unique feature that was not shared by distractors. In the attentive search task, targets lacked a feature that was present in the distractors. Preattentive search was normal in 3 neglect patients with cortical lesions but not in 2 neglect patients with hemianopia. A 4th neglect patient without hemianopia with a subcortical infarct abnormally used serial search mechanisms in the preattentive task. Neglect patients were characteristically impaired in the contralesional field in the attentive search task. This study demonstrates preserved explicit detection of visual features in cases of hemispatial neglect.

Dynamic Brain Network Correlates of Spontaneous Fluctuations in Attention

Abstract Human attention is intrinsically dynamic, with focus continuously shifting between elements of the external world and internal, self‐generated thoughts. Communication within and between large‐scale brain networks also fluctuates spontaneously from moment to moment. However, the behavioral relevance of dynamic functional connectivity and possible link with attentional state shifts is unknown. We used a unique approach to examine whether brain network dynamics reflect spontaneous fluctuations in moment‐to‐moment behavioral variability, a sensitive marker of attentional state. Nineteen healthy adults were instructed to tap their finger every 600 ms while undergoing fMRI. This novel, but simple, approach allowed us to isolate moment‐to‐moment fluctuations in behavioral variability related to attention, independent of common confounds in cognitive tasks (e.g., stimulus changes, response inhibition). Spontaneously increasing tap variance (“out‐of‐the‐zone” attention) was associated with increasing activation in dorsal‐attention and salience network regions, whereas decreasing tap variance (“in‐the‐zone” attention) was marked by increasing activation of default mode network (DMN) regions. Independent of activation, tap variance representing out‐of‐the‐zone attention was also time‐locked to connectivity both within DMN and between DMN and salience network regions. These results provide novel mechanistic data on the understudied neural dynamics of everyday, moment‐to‐moment attentional fluctuations, elucidating the behavioral importance of spontaneous, transient coupling within and between attention‐relevant networks.

Visual Hemispatial Neglect, Re-Assessed

Increased computer use in clinical settings offers an opportunity to develop new neuropsychological tests that exploit the control computers have over stimulus dimensions and timing. However, before adopting new tools, empirical validation is necessary. In the current study, our aims were twofold: to describe a computerized adaptive procedure with broad potential for neuropsychological investigations, and to demonstrate its implementation in testing for visual hemispatial neglect. Visual search results from adaptive psychophysical procedures are reported from 12 healthy individuals and 23 individuals with unilateral brain injury. Healthy individuals reveal spatially symmetric performance on adaptive search measures. In patients, psychophysical outcomes (as well as those from standard paper-and-pencil search tasks) reveal visual hemispatial neglect. Consistent with previous empirical studies of hemispatial neglect, lateralized impairments in adaptive conjunction search are greater than in adaptive feature search tasks. Furthermore, those with right hemisphere damage show greater lateralized deficits in conjunction search than do those with left hemisphere damage. We argue that adaptive tests, which automatically adjust to each individuals performance level, are efficient methods for both clinical evaluations and neuropsychological investigations and have the potential to detect subtle deficits even in chronic stages, when flagrant clinical signs have frequently resolved.