Radek Ptak

The Frontoparietal Attention Network of the Human Brain: Action, Saliency, and a Priority Map of the Environment

The dorsal convexity of the human frontal and parietal lobes forms a network that is crucially involved in the selection of sensory contents by attention. This network comprehends cortex along the intraparietal sulcus, the inferior parietal lobe, and dorsal premotor cortex, including the frontal eye field. These regions are richly interconnected with recurrent fibers passing through the superior longitudinal fasciculus. The posterior parietal cortex has several functional characteristics—such as feature-independent coding, enhancement of activity by attention, representation of task-related signals, and access to multiple reference frames—that point to a central role of this region in the computation of a feature- and modality-independent priority map of the environment. The priority map integrates feature information elaborated in sensory cortex and top-down representations of behavioral goals and expectations originating in the dorsolateral prefrontal and premotor cortex. This review presents converging evidence from single-unit studies of the primate brain, functional neuroimaging, and investigations of neuropsychological disorders such as Bálint syndrome and spatial neglect for a decisive role of the frontoparietal attention network in the selection of relevant environmental information.

Decision-making in amnesia: do advantageous decisions require conscious knowledge of previous behavioural choices?

Previous work has reported that in the Iowa gambling task (IGT) advantageous decisions may be taken before the advantageous strategy is known [Bechara, A., Damasio, H., Tranel, D., & Damasio, A. R. (1997). Deciding advantageously before knowing the advantageous strategy. Science, 275, 1293-1295]. In order to test whether explicit memory is essential for the acquisition of a behavioural preference for advantageous choices, we measured behavioural performance and skin conductance responses (SCRs) in five patients with dense amnesia following damage to the basal forebrain and orbitofrontal cortex, six amnesic patients with damage to the medial temporal lobe or the diencephalon, and eight control subjects performing the IGT. Across 100 trials healthy participants acquired a preference for advantageous choices and generated large SCRs to high levels of punishment. In addition, their anticipatory SCRs to disadvantageous choices were larger than to advantageous choices. However, this dissociation occurred much later than the behavioural preference for advantageous alternatives. In contrast, though exhibiting discriminatory autonomic SCRs to different levels of punishment, 9 of 11 amnesic patients performed at chance and did not show differential anticipatory SCRs to advantageous and disadvantageous choices. Further, the magnitude of anticipatory SCRs did not correlate with behavioural performance. These results suggest that the acquisition of a behavioural preference--be it for advantageous or disadvantageous choices--depends on the memory of previous reinforcements encountered in the task, a capacity requiring intact explicit memory.

The Dorsal Attention Network Mediates Orienting toward Behaviorally Relevant Stimuli in Spatial Neglect

Experimental neurophysiology and functional neuroimaging have identified a dorsal attention network that encodes neural signals related to the behavioral significance of a stimulus. The core anatomical areas of this network are the frontal eye fields and the posterior parietal cortex, which are interconnected by the superior longitudinal fasciculus. Here, we show that damage or disconnection of this network predicts the extent to which task-relevant stimuli capture attention of human stroke patients with spatial neglect. Healthy volunteers, right-hemisphere-damaged control participants, and patients with left neglect reacted to peripheral targets defined by their color, which were preceded by a brief distracter stimulus. The position of the distracter and its relevance for the current trial were independently varied. In neglect patients with damage including the frontal eye fields and the superior longitudinal fasciculus, ipsilesional distracters impaired orienting into contralesional space regardless of their relevance for the current task. In contrast, patients with sparing of these regions were only impaired when distracters were task-relevant. These findings indicate that the dorsal attention network controls spatial orienting by modulating the saliency of distracter stimuli according to current action goals.

The behavioral significance of coherent resting-state oscillations after stroke

Stroke lesions induce not only loss of local neural function, but disruptions in spatially distributed areas. However, it is unknown whether they affect the synchrony of electrical oscillations in neural networks and if changes in network coherence are associated with neurological deficits. This study assessed these questions in a population of patients with subacute, unilateral, ischemic stroke. Spontaneous cortical oscillations were reconstructed from high-resolution electroencephalograms (EEG) with adaptive spatial filters. Maps of functional connectivity (FC) between brain areas were created and correlated with patient performance in motor and cognitive scores. In comparison to age matched healthy controls, stroke patients showed a selective disruption of FC in the alpha frequency range. The spatial distribution of alpha band FC reflected the pattern of motor and cognitive deficits of the individual patient: network nodes that participate normally in the affected functions showed local decreases in FC with the rest of the brain. Interregional FC in the alpha band, but not in delta, theta, or beta frequencies, was highly correlated with motor and cognitive performance. In contrast, FC between contralesional areas and the rest of the brain was negatively associated with patient performance. Alpha oscillation synchrony at rest is a unique and specific marker of network function and linearly associated with behavioral performance. Maps of alpha synchrony computed from a single resting-state EEG recording provide a robust and convenient window into the functionality and organization of cortical networks with numerous potential applications.

The attention network of the human brain: relating structural damage associated with spatial neglect to functional imaging correlates of spatial attention

Functional imaging studies of spatial attention regularly report activation of the intraparietal sulcus (IPS) and dorsal premotor cortex including the frontal eye fields (FEF) in tasks requiring overt or covert shifting of attention. In contrast, lesion-overlap studies of patients with spatial neglect - a syndrome characterized by severe impairments of spatial attention - show that the critical damage concerns more ventral regions, comprising the inferior parietal lobule, the temporal-parietal junction (TPJ), and the superior temporal gyrus. We performed voxel-based lesion-symptom mapping of 29 right-hemisphere stroke patients, using several performance indices derived from a cueing task as measures of spatial attention. In contrast to previous studies, we focused our analyses on eight regions of interest defined according to results of previous functional imaging studies. A direct comparison of neglect with control patients revealed that neglect was associated with damage to the TPJ, the middle frontal gyrus, and the posterior IPS. The latter region was also a significant predictor of the degree of contralesional slowing of target detection and the extent to which ipsilesional distracters captured attention of neglect patients. Finally, damage to the FEF and posterior IPS was negatively correlated with the tendency of neglect patients to orient attention toward behaviourally relevant distracters. These findings support the results of functional imaging studies of spatial attention and provide evidence for a network account of neglect, according to which attentional selection of relevant environmental stimuli and the reorienting of attention result from dynamic interactions between the IPS, the dorsal premotor cortex, and the TPJ.

Cortical and subcortical anatomy of chronic spatial neglect following vascular damage.

BackgroundThe role of the inferior parietal lobule (IPL) and superior temporal gyrus (STG) or subcortical pathways as possible anatomical correlates of spatial neglect is currently intensely discussed. Some of the conflicting results might have arisen because patients were examined in the acute stage of disease.MethodsWe examined the anatomical basis of spatial neglect in a sample of patients examined in the post-acute stage following right-hemispheric vascular brain damage. Lesions of 28 patients with chronic spatial neglect were contrasted to lesions of 22 control patients without neglect using lesion subtraction techniques and voxel-wise comparisons.ResultsThe comparisons identified the temporo-parietal junction (TPJ) with underlying white matter, the supramarginal gyrus, the posterior STG, and the insula as brain regions damaged significantly more often in neglect compared to non-neglect patients. In a subgroup of neglect patients showing particularly large cancellation bias together with small errors on line bisection damage was prevalent deep in the frontal lobe while damage of patients with the reverse pattern was located in the white matter of the TPJ.ConclusionConsidering our results and the findings of previous studies, spatial neglect appears to be associated with a network of regions involving the TPJ, inferior IPL, posterior STG, the insular cortex, and posterior-frontal projections. Frontal structures or projections may be of particular relevance for spatial exploration, while the IPL may be important for object-based attention as required for line bisection.

The space of senses: impaired crossmodal interactions in a patient with Balint syndrome after bilateral parietal damage

Balint syndrome after bilateral parietal damage involves a severe disturbance of space representation including impaired oculomotor behaviour, optic ataxia, and simultanagnosia. Binding of object features into a unique spatial representation can also be impaired. We report a patient with bilateral parietal lesions and Balint syndrome, showing severe spatial deficits in several visual tasks predominantly affecting the left hemispace. In particular, we tested whether a loss of spatial representation would affect crossmodal interactions between simultaneous visual and tactile events occurring at the same versus different locations. A tactile discrimination task, where spatially congruent or incongruent visual cues were delivered near the patients hands, was used. Following stimulation of the left hand in the left side of space, we observed visuo-tactile interactions that were not modulated by spatially congruent conditions. In contrast, performance following stimulation of the right hand in the right side of space was affected in a spatially selective manner--facilitated for congruent stimuli and slowed for incongruent stimuli. To dissociate effects on somatotopic and spatiotopic coordinates, we crossed the patients hands during unimodal tactile discriminations. Tactile performance of the left hand improved when it was positioned in the right hemispace, whereas placing the right hand in left space produced no significant changes, suggesting that left-sided tactile inputs are coded with respect to a combination of limb- and trunk-centred coordinates. These data converge with recent findings in animals and healthy humans to indicate a critical role of the posterior parietal cortex in multimodal spatial integration, and in the fusion of different coordinates into a unified representation of space.

Decoupling of autonomic and cognitive emotional reactions after cerebellar stroke.

Emotional blunting can be found after cerebellar lesions. However, the mechanism of such a modification is not clear. We present a patient with emotional flattening and increased risk taking after left cerebellar infarct who had an impaired autonomic reactivity to negative as compared with positive reinforcement. This impairment was demonstrated by the patients undifferentiated skin conductance responses to negative and positive reinforcement, whereas controls produced larger skin conductance responses after negative feedback. The cooccurrence of emotional flattening and undifferentiated autonomic reactions to positively and negatively valenced stimuli strengthens the role of the cerebellum in the modulation of the autonomic responses. Ann Neurol 2003;53:654–658

Spontaneous confabulations after Orbitofrontal damage: The role of temporal context confusion and self-monitoring

Abstract Orbitofrontal damage or disconnection may lead to spontaneous confabulations, which have the meaning of reality for the patients and occasionally motivate them to act. Spontaneous confabulations are based on a temporal confusion of diverse experiences in memory, i.e. increased temporal context confusion (TCC). Here, we report a patient who suffered orbitofrontal and basal forebrain damage after haemorrhage from an anterior communicating artery aneurysm. The patient was severely amnesic and confabulated spontaneously. His confabulations could always be traced back to actual experiences, an observation indicating a confusion of temporal context in memory. In a recognition task measuring TCC in which all our previous spontaneous confabulators had failed, the patient appeared to use an uncommonly stringent recognition criterion suggestive of attempted, wilful self-monitoring. Only when he was motivated to improve his recognition performance did increased TCC became measurable. In non-confabulating am...

Forms of confabulation: Dissociations and associations

Confabulation denotes the emergence of memories of experiences and events which never took place. Whether there are distinct forms with distinct mechanisms is still debated. In this study, we explored 4 forms of confabulation and their mechanisms in 29 amnesic patients. Patients performed tests of explicit memory, executive functions, and two test of orbitofrontal reality filtering (memory selection and extinction capacity in a reversal learning task) previously shown to be strongly associated with confabulations that patients act upon and disorientation. Results indicated the following associations: (1) Intrusions in a verbal memory test (simple provoked confabulations) dissociated from all other forms of confabulation and were not associated with any specific cognitive measure. (2) Momentary confabulations, defined as confabulatory responses to questions and measured with a confabulation questionnaire, were associated with impaired mental flexibility, a tendency to fill gaps in memory, and with one measure of reality filtering. Momentary confabulations, therefore, may emanate from diverse causes. (3) Behaviourally spontaneous confabulation, characterized by confabulations that the patients act upon and disorientation, was strongly associated with failure in the two reality filtering tasks. Behaviourally spontaneous confabulation may be seen as a specific instance of momentary confabulations with a distinct mechanism. (4) A patient producing fantastic confabulations with nonsensical, illogical content had wide-spread cognitive dysfunction and failed in the reality filtering tasks. The results support the presence of truly or partially dissociable types of confabulation with different mechanisms.