Alexandra Woolgar

Executive function and fluid intelligence after frontal lobe lesions.

Many tests of specific ‘executive functions’ show deficits after frontal lobe lesions. These deficits appear on a background of reduced fluid intelligence, best measured with tests of novel problem solving. For a range of specific executive tests, we ask how far frontal deficits can be explained by a general fluid intelligence loss. For some widely used tests, e.g. Wisconsin Card Sorting, we find that fluid intelligence entirely explains frontal deficits. When patients and controls are matched on fluid intelligence, no further frontal deficit remains. For these tasks too, deficits are unrelated to lesion location within the frontal lobe. A second group of tasks, including tests of both cognitive (e.g. Hotel, Proverbs) and social (Faux Pas) function, shows a different pattern. Deficits are not fully explained by fluid intelligence and the data suggest association with lesions in the right anterior frontal cortex. Understanding of frontal lobe deficits may be clarified by separating reduced fluid intelligence, important in most or all tasks, from other more specific impairments and their associated regions of damage.

Fluid intelligence loss linked to restricted regions of damage within frontal and parietal cortex

Tests of fluid intelligence predict success in a wide range of cognitive activities. Much uncertainty has surrounded brain lesions producing deficits in these tests, with standard group comparisons delivering no clear result. Based on findings from functional imaging, we propose that the uncertainty of lesion data may arise from the specificity and complexity of the relevant neural circuit. Fluid intelligence tests give a characteristic pattern of activity in posterolateral frontal, dorsomedial frontal, and midparietal cortex. To test the causal role of these regions, we examined fluid intelligence in 80 patients with focal cortical lesions. Damage to each of the proposed regions predicted fluid intelligence loss, whereas damage outside these regions was not predictive. The results suggest that coarse group comparisons (e.g., frontal vs. posterior) cannot show the neural underpinnings of fluid intelligence tests. Instead, deficits reflect the extent of damage to a restricted but complex brain circuit comprising specific regions within both frontal and posterior cortex.

Adaptive coding of task-relevant information in human frontoparietal cortex.

Frontoparietal cortex is thought to be essential for flexible behavior, but the mechanism for control remains elusive. Here, we demonstrate a potentially critical property of this cortex: its dynamic configuration for coding of task-critical information. Using multivoxel pattern analysis of human functional imaging data, we demonstrate an adaptive change in the patterns of activation coding task-relevant stimulus distinctions. When task demands made perceptual information more difficult to discriminate, frontoparietal regions showed increased coding of this information. Visual cortices showed the opposite result: a weaker representation of perceptual information in line with the physical change in the stimulus. On a longer timescale, a rebalancing of coding was also seen after practice, with a diminished representation of task rules as they became familiar. The results suggest a flexible neural system, exerting cognitive control in a wide range of tasks by adaptively representing the task features most challenging for successful goal-directed behavior.

Multi-voxel coding of stimuli, rules, and responses in human frontoparietal cortex.

In human functional magnetic resonance imaging (fMRI), a characteristic pattern of frontal and parietal activity is produced by many different cognitive demands. Although frontoparietal cortex has been shown to represent a variety of task features in different contexts, little is known about detailed representation of different task features within and across different regions. We used multi-voxel pattern analysis (MVPA) of human fMRI data to assess the representational content of frontoparietal cortex in a simple stimulus-response task. Stimulus-response mapping rule was the most strongly represented task feature, significantly coded in a lateral frontal region surrounding the inferior frontal sulcus, a more ventral region including the anterior insula/frontal operculum, and the intraparietal sulcus. Next strongest was coding of the instruction cue (screen color) indicating which rule should be applied. Coding of individual stimuli and responses was weaker, approaching significance in a subset of regions. In line with recent single unit data, the results show a broad representation of task-relevant information across human frontoparietal cortex, with strong representation of a general rule or cognitive context, and weaker coding of individual stimulus/response instances.

The role of Area 10 (BA10) in human multitasking and in social cognition: a lesion study.

A role for rostral prefrontal cortex (BA10) has been proposed in multitasking, in particular, the selection and maintenance of higher order internal goals while other sub-goals are being performed. BA10 has also been implicated in the ability to infer someone elses feelings and thoughts, often referred to as theory of mind. While most of the data to support these views come from functional neuroimaging studies, lesion studies are scant. In the present study, we compared the performance of a group of frontal patients whose lesions involved BA10, a group of frontal patients whose lesions did not affect this area (nonBA10), and a group of healthy controls on tests requiring multitasking and complex theory of mind judgments. Only the group with lesions involving BA10 showed deficits on multitasking and theory of mind tasks when compared with control subjects. NonBA10 patients performed more poorly than controls on an executive function screening tool, particularly on measures of response inhibition and abstract reasoning, suggesting that theory of mind and multitasking deficits following lesions to BA10 cannot be explained by a general worsening of executive function. In addition, we searched for correlations between performance and volume of damage within different subregions of BA10. Significant correlations were found between multitasking performance and volume of damage in right lateral BA10, and between theory of mind and total BA10 lesion volume. These findings stress the potential pivotal role of BA10 in higher order cognitive functions.

A frontotemporoparietal network common to initiating and responding to joint attention bids

Joint attention is a fundamental cognitive ability that supports daily interpersonal relationships and communication. The Parallel Distributed Processing model (PDPM) postulates that responding to (RJA) and initiating (IJA) joint attention are predominantly supported by posterior-parietal and frontal regions respectively. It also argues that these neural networks integrate during development, supporting the parallel processes of self- and other-attention representation during interactions. However, direct evidence for the PDPM is limited due to a lack of ecologically valid experimental paradigms that can capture both RJA and IJA. Building on existing interactive approaches, we developed a virtual reality paradigm where participants engaged in an online interaction to complete a cooperative task. By including tightly controlled baseline conditions to remove activity associated with non-social task demands, we were able to directly contrast the neural correlates of RJA and IJA to determine whether these processes are supported by common brain regions. Both RJA and IJA activated broad frontotemporoparietal networks. Critically, a conjunction analysis identified that a subset of these regions were common to both RJA and IJA. This right-lateralised network included the dorsal portion of the middle frontal gyrus (MFG), inferior frontal gyrus (IFG), middle temporal gyrus (MTG), precentral gyrus, posterior superior temporal sulcus (pSTS), temporoparietal junction (TPJ) and precuneus. Additional activation was observed in this network for IJA relative to RJA at MFG, IFG, TPJ and precuneus. This is the first imaging study to directly investigate the neural correlates common to RJA and IJA engagement, and thus support the assumption that a broad integrated network underlies the parallel aspects of both initiating and responding to joint attention.

Multi-voxel pattern analysis (MVPA) reveals abnormal fMRI activity in both the "core" and "extended" face network in congenital prosopagnosia.

The ability to identify faces is mediated by a network of cortical and subcortical brain regions in humans. It is still a matter of debate which regions represent the functional substrate of congenital prosopagnosia (CP), a condition characterized by a lifelong impairment in face recognition, and affecting around 2.5% of the general population. Here, we used functional Magnetic Resonance Imaging (fMRI) to measure neural responses to faces, objects, bodies, and body-parts in a group of seven CPs and ten healthy control participants. Using multi-voxel pattern analysis (MVPA) of the fMRI data we demonstrate that neural activity within the “core” (i.e., occipital face area and fusiform face area) and “extended” (i.e., anterior temporal cortex) face regions in CPs showed reduced discriminability between faces and objects. Reduced differentiation between faces and objects in CP was also seen in the right parahippocampal cortex. In contrast, discriminability between faces and bodies/body-parts and objects and bodies/body-parts across the ventral visual system was typical in CPs. In addition to MVPA analysis, we also ran traditional mass-univariate analysis, which failed to show any group differences in face and object discriminability. In sum, these findings demonstrate (i) face-object representations impairments in CP which encompass both the “core” and “extended” face regions, and (ii) superior power of MVPA in detecting group differences.

Attention enhances multi-voxel representation of novel objects in frontal, parietal and visual cortices

Selective attention is fundamental for human activity, but the details of its neural implementation remain elusive. One influential theory, the adaptive coding hypothesis (Duncan, 2001, An adaptive coding model of neural function in prefrontal cortex, Nature Reviews Neuroscience 2:820-829), proposes that single neurons in certain frontal and parietal regions dynamically adjust their responses to selectively encode relevant information. This selective representation may in turn support selective processing in more specialized brain regions such as the visual cortices. Here, we use multi-voxel decoding of functional magnetic resonance images to demonstrate selective representation of attended--and not distractor--objects in frontal, parietal, and visual cortices. In addition, we highlight a critical role for task demands in determining which brain regions exhibit selective coding. Strikingly, representation of attended objects in frontoparietal cortex was highest under conditions of high perceptual demand, when stimuli were hard to perceive and coding in early visual cortex was weak. Coding in early visual cortex varied as a function of attention and perceptual demand, while coding in higher visual areas was sensitive to the allocation of attention but robust to changes in perceptual difficulty. Consistent with high-profile reports, peripherally presented objects could also be decoded from activity at the occipital pole, a region which corresponds to the fovea. Our results emphasize the flexibility of frontoparietal and visual systems. They support the hypothesis that attention enhances the multi-voxel representation of information in the brain, and suggest that the engagement of this attentional mechanism depends critically on current task demands.

Representational dynamics of object recognition: Feedforward and feedback information flows

Object perception involves a range of visual and cognitive processes, and is known to include both a feedfoward flow of information from early visual cortical areas to higher cortical areas, along with feedback from areas such as prefrontal cortex. Previous studies have found that low and high spatial frequency information regarding object identity may be processed over different timescales. Here we used the high temporal resolution of magnetoencephalography (MEG) combined with multivariate pattern analysis to measure information specifically related to object identity in peri-frontal and peri-occipital areas. Using stimuli closely matched in their low-level visual content, we found that activity in peri-occipital cortex could be used to decode object identity from ~80ms post stimulus onset, and activity in peri-frontal cortex could also be used to decode object identity from a later time (~265ms post stimulus onset). Low spatial frequency information related to object identity was present in the MEG signal at an earlier time than high spatial frequency information for peri-occipital cortex, but not for peri-frontal cortex. We additionally used Granger causality analysis to compare feedforward and feedback influences on representational content, and found evidence of both an early feedfoward flow and later feedback flow of information related to object identity. We discuss our findings in relation to existing theories of object processing and propose how the methods we use here could be used to address further questions of the neural substrates underlying object perception.

Flexible coding of task rules in frontoparietal cortex: An adaptive system for flexible cognitive control

How do our brains achieve the cognitive control that is required for flexible behavior? Several models of cognitive control propose a role for frontoparietal cortex in the structure and representation of task sets or rules. For behavior to be flexible, however, the system must also rapidly reorganize as mental focus changes. Here we used multivoxel pattern analysis of fMRI data to demonstrate adaptive reorganization of frontoparietal activity patterns following a change in the complexity of the task rules. When task rules were relatively simple, frontoparietal cortex did not hold detectable information about these rules. In contrast, when the rules were more complex, frontoparietal cortex showed clear and decodable rule discrimination. Our data demonstrate that frontoparietal activity adjusts to task complexity, with better discrimination of rules that are behaviorally more confusable. The change in coding was specific to the rule element of the task and was not mirrored in more specialized cortex (early visual cortex) where coding was independent of difficulty. In line with an adaptive view of frontoparietal function, the data suggest a system that rapidly reconfigures in accordance with the difficulty of a behavioral task. This system may provide a neural basis for the flexible control of human behavior.