Task phase-specific involvement of the rat posterior parietal cortex in performance of the TUNL task

The posterior parietal cortex (PPC) participates in cognitive processes including working memory (WM), sensory evidence accumulation, and perceptually guided decision making. However, surprisingly little work has used temporally precise manipulations to dissect its role in different epochs of behavior taking place over short timespans, such as WM tasks. As a result, a consistent view of the temporally precise role of the PPC in these processes has not been described. In the present study, we investigated the temporally specific role of the PPC in the Trial-Unique, Nonmatching-to-Location (TUNL) task, a touchscreen-based, visuospatial WM task that relies on the PPC. To disrupt PPC activity in a temporally precise manner, we applied mild intracranial electrical stimulation (ICES). We found that intra-PPC ICES (100 μA) significantly impaired accuracy in TUNL without significantly altering response latency. Moreover, we found that the impairment was specific to ICES applied during the delay and test phases of TUNL. Consistent with previous reports showing delay- and choice-specific neuronal activity in the PPC, the results provide evidence that the rat PPC is required for maintaining memory representations of stimuli over a delay period as well as for making successful comparisons and choices between test stimuli. In contrast, the PPC appears not to be critical for initial encoding of sample stimuli. This pattern of results may indicate that early encoding of visual stimuli is independent of the PPC or that the PPC becomes engaged only when visual stimuli are spatially complex or involve memory or decision making.     

Fix your eyes in the space you could reach: neurons in the macaque medial parietal cortex prefer gaze positions in peripersonal space

Interacting in the peripersonal space requires coordinated arm and eye movements to visual targets in depth. In primates, the medial posterior parietal cortex (PPC) represents a crucial node in the process of visual-to-motor signal transformations. The medial PPC area V6A is a key region engaged in the control of these processes because it jointly processes visual information, eye position and arm movement related signals. However, to date, there is no evidence in the medial PPC of spatial encoding in three dimensions. Here, using single neuron recordings in behaving macaques, we studied the neural signals related to binocular eye position in a task that required the monkeys to perform saccades and fixate targets at different locations in peripersonal and extrapersonal space. A significant proportion of neurons were modulated by both gaze direction and depth, i.e., by the location of the foveated target in 3D space. The population activity of these neurons displayed a strong preference for peripersonal space in a time interval around the saccade that preceded fixation and during fixation as well. This preference for targets within reaching distance during both target capturing and fixation suggests that binocular eye position signals are implemented functionally in V6A to support its role in reaching and grasping.     

The Importance of Lateral Connections in the Parietal Cortex for Generating Motor Plans

Substantial evidence has highlighted the significant role of associative brain areas, such as the posterior parietal cortex (PPC) in transforming multimodal sensory information into motor plans. However, little is known about how different sensory information, which can have different delays or be absent, combines to produce a motor plan, such as executing a reaching movement. To address these issues, we constructed four biologically plausible network architectures to simulate PPC: 1) feedforward from sensory input to the PPC to a motor output area, 2) feedforward with the addition of an efference copy from the motor area, 3) feedforward with the addition of lateral or recurrent connectivity across PPC neurons, and 4) feedforward plus efference copy, and lateral connections. Using an evolutionary strategy, the connectivity of these network architectures was evolved to execute visually guided movements, where the target stimulus provided visual input for the entirety of each trial. The models were then tested on a memory guided motor task, where the visual target disappeared after a short duration. Sensory input to the neural networks had sensory delays consistent with results from monkey studies. We found that lateral connections within the PPC resulted in smoother movements and were necessary for accurate movements in the absence of visual input. The addition of lateral connections resulted in velocity profiles consistent with those observed in human and non-human primate visually guided studies of reaching, and allowed for smooth, rapid, and accurate movements under all conditions. In contrast, Feedforward or Feedback architectures were insufficient to overcome these challenges. Our results suggest that intrinsic lateral connections are critical for executing accurate, smooth motor plans.     

Crossmodal processing of object features in human anterior intraparietal cortex: an fMRI study implies equivalencies between humans and monkeys

The organization of macaque posterior parietal cortex (PPC) reflects its functional specialization in integrating polymodal sensory information for object recognition and manipulation. Neuropsychological and recent human imaging studies imply equivalencies between human and macaque PPC, and in particular, the cortex buried in the intraparietal sulcus (IPS). Using functional MRI, we tested the hypothesis that an area in human anterior intraparietal cortex is activated when healthy subjects perform a crossmodal visuo-tactile delayed matching-to-sample task with objects. Tactile or visual object presentation (encoding and recognition) both significantly activated anterior intraparietal cortex. As hypothesized, neural activity in this area was further enhanced when subjects transferred object information between modalities (crossmodal matching). Based on both the observed functional properties and the anatomical location, we suggest that this area in anterior IPS is the human equivalent of macaque area AIP.     

Posterior parietal cortex: Space--and beyond

How do we decide how to react to a stimulus or event? To do so requires recognition of the stimulus itself as well as an appreciation of the context within which that stimulus is encountered. In this issue of Neuron, Stoet and Snyder report that neurons in the parietal cortex of monkeys can carry contextual information related to the rules that are relevant for solving a visual discrimination task.     

Top-down control-signal dynamics in anterior cingulate and prefrontal cortex neurons following task switching

The prefrontal cortex (PFC) and anterior cingulate cortex (ACC) have both been implicated in cognitive control, but their relative roles remain unclear. Here we recorded the activity of single neurons in both areas while monkeys performed a task that required them to switch between trials in which they had to look toward a flashed stimulus (prosaccades) and trials in which they had to look away from the stimulus (antisaccades). We found that ACC neurons had a higher level of task selectivity than PFC neurons during the preparatory period on trials immediately following a task switch. In ACC neurons, task selectivity was strongest after the task switch and declined throughout the task block, whereas task selectivity remained constant in the PFC. These results demonstrate that the ACC is recruited when cognitive demands increase and suggest a role for both areas in task maintenance and the implementation of top-down control.     

Maps of space in human frontoparietal cortex

Prefrontal cortex (PFC) and posterior parietal cortex (PPC) are neural substrates for spatial cognition. We here review studies in which we tested the hypothesis that human frontoparietal cortex may function as a priority map. According to priority map theory, objects or locations in the visual world are represented by neural activity that is proportional to their attentional priority. Using functional magnetic resonance imaging (fMRI), we first identified topographic maps in PFC and PPC as candidate priority maps of space. We then measured fMRI activity in candidate priority maps during the delay periods of a covert attention task, a spatial working memory task, and a motor planning task to test whether the activity depended on the particular spatial cognition. Our hypothesis was that some, but not all, candidate priority maps in PFC and PPC would be agnostic with regard to what was being prioritized, in that their activity would reflect the location in space across tasks rather than a particular kind of spatial cognition (e.g., covert attention). To test whether patterns of delay period activity were interchangeable during the spatial cognitive tasks, we used multivariate classifiers. We found that decoders trained to predict the locations on one task (e.g., working memory) cross-predicted the locations on the other tasks (e.g., covert attention and motor planning) in superior precentral sulcus (sPCS) and in a region of intraparietal sulcus (IPS2), suggesting that these patterns of maintenance activity may be interchangeable across the tasks. Such properties make sPCS in frontal cortex and IPS2 in parietal cortex viable priority map candidates, and suggest that these areas may be the human homologs of the monkey frontal eye field (FEF) and lateral intraparietal area (LIP).     

Craniotopic updating of visual space across saccades in the human posterior parietal cortex

The neural mechanisms underlying the craniotopic updating of visual space across saccadic eye movements are poorly understood. Previous single-unit recording studies in primates and clinical studies in brain-damaged patients have shown that the posterior parietal cortex (PPC) has a key role in this process. In the present study, we used single-pulse transcranial magnetic stimulation (TMS) to disrupt the processing within the PPC during a task that requires craniotopic updating: double saccades. In this task, two targets are presented in quick succession and the subject is required to make a saccade to each location as accurately as possible. We show here that TMS delivered to the PPC just prior to the second saccade effectively disrupts the craniotopic coding normally observed in this task. This causes subjects to revert to saccades more consistent with a representation of the targets based on their positions relative to one another. By contrast, stimulation at earlier times between the two saccades did not disrupt performance. These results suggest that extraretinal information generated during the first perisaccadic period is not put into functional use until just prior to the second saccade.     

Dissociation between Dorsal and Ventral Posterior Parietal Cortical Responses to Incidental Changes in Natural Scenes

Background

The posterior parietal cortex (PPC) is thought to interact with the medial temporal lobe (MTL) to support spatial cognition and topographical memory. While the response of medial temporal lobe regions to topographical stimuli has been intensively studied, much less research has focused on the role of PPC and its functional connectivity with the medial temporal lobe.

Methodology/Principle Findings

Here we report a dissociation between dorsal and ventral regions of PPC in response to different types of change in natural scenes using an fMRI adaptation paradigm. During scanning subjects performed an incidental target detection task whilst viewing trial unique sequentially presented pairs of natural scenes, each containing a single prominent object. We observed a dissociation between the superior parietal gyrus and the angular gyrus, with the former showing greater sensitivity to spatial change, and the latter showing greater sensitivity to scene novelty. In addition, we observed that the parahippocampal cortex has increased functional connectivity with the angular gyrus, but not superior parietal gyrus, when subjects view change to the scene content.

Conclusions/Significance

Our findings provide support for proposed dissociations between dorsal and ventral regions of PPC and suggest that the dorsal PPC may support the spatial coding of the visual environment even when this information is incidental to the task at hand. Further, through revealing the differential functional interactions of the SPG and AG with the MTL our results help advance our understanding of how the MTL and PPC cooperate to update representations of the world around us.     

Spatial and non-spatial functions of the parietal cortex

Although the parietal cortex is traditionally associated with spatial attention and sensorimotor integration, recent evidence also implicates it in higher order cognitive functions. We review relevant results from neuron recording studies showing that inferior parietal neurons integrate information regarding target location with a variety of non-spatial signals. Some of these signals are modulatory and alter a stimulus-evoked response according to the action, category, or reward associated with the stimulus. Other non-spatial inputs act independently, encoding the context or rules of a task even before the presentation of a specific target. Despite the ubiquity of non-spatial information in individual neurons, reversible inactivation of the parietal lobe affects only spatial orienting of attention and gaze, but not non-spatial aspects of performance. This suggests that non-spatial signals contribute to an underlying spatial computation, possibly allowing the brain to determine which targets are worthy of attention or action in a given task context.     

Prefrontal cortex and neural mechanisms of executive function

Executive function is a product of the coordinated operation of multiple neural systems and an essential prerequisite for a variety of cognitive functions. The prefrontal cortex is known to be a key structure for the performance of executive functions. To accomplish the coordinated operations of multiple neural systems, the prefrontal cortex must monitor the activities in other cortical and subcortical structures and control and supervise their operations by sending command signals, which is called top-down signaling. Although neurophysiological and neuroimaging studies have provided evidence that the prefrontal cortex sends top-down signals to the posterior cortices to control information processing, the neural correlate of these top-down signals is not yet known. Through use of the paired association task, it has been demonstrated that top-down signals are used to retrieve specific information stored in long-term memory. Therefore, we used a paired association task to examine the neural correlates of top-down signals in the prefrontal cortex. The preliminary results indicate that 32% of visual neurons exhibit pair-selectivity, which is similar to the characteristics of pair-coding activities in temporal neurons. The latency of visual responses in prefrontal neurons was longer than bottom-up signals but faster than top-down signals in inferior temporal neurons. These results suggest that pair-selective visual responses may be top-down signals that the prefrontal cortex provides to the temporal cortex, although further studies are needed to elucidate the neural correlates of top-down signals and their characteristics to understand the neural mechanism of executive control by the prefrontal cortex.     

Neuronal Correlates of Cognitive Control during Gaming Revealed by Near-Infrared Spectroscopy

In everyday life we quickly build and maintain associations between stimuli and behavioral responses. This is governed by rules of varying complexity and past studies have identified an underlying fronto-parietal network involved in cognitive control processes. However, there is only limited knowledge about the neuronal activations during more natural settings like game playing. We thus assessed whether near-infrared spectroscopy recordings can reflect different demands on cognitive control during a simple game playing task. Sixteen healthy participants had to catch falling objects by pressing computer keys. These objects either fell randomly (RANDOM task), according to a known stimulus-response mapping applied by players (APPLY task) or according to a stimulus-response mapping that had to be learned (LEARN task). We found an increased change of oxygenated and deoxygenated hemoglobin during LEARN covering broad areas over right frontal, central and parietal cortex. Opposed to this, hemoglobin changes were less pronounced for RANDOM and APPLY. Along with the findings that fewer objects were caught during LEARN but stimulus-response mappings were successfully identified, we attribute the higher activations to an increased cognitive load when extracting an unknown mapping. This study therefore demonstrates a neuronal marker of cognitive control during gaming revealed by near-infrared spectroscopy recordings.     

Transcranial Electrical Stimulation over Dorsolateral Prefrontal Cortex Modulates Processing of Social Cognitive and Affective Information

Recent neurofunctional studies suggested that lateral prefrontal cortex is a domain-general cognitive control area modulating computation of social information. Neuropsychological evidence reported dissociations between cognitive and affective components of social cognition. Here, we tested whether performance on social cognitive and affective tasks can be modulated by transcranial direct current stimulation (tDCS) over dorsolateral prefrontal cortex (DLPFC). To this aim, we compared the effects of tDCS on explicit recognition of emotional facial expressions (affective task), and on one cognitive task assessing the ability to adopt another person’s visual perspective. In a randomized, cross-over design, male and female healthy participants performed the two experimental tasks after bi-hemispheric tDCS (sham, left anodal/right cathodal, and right anodal/left cathodal) applied over DLPFC. Results showed that only in male participants explicit recognition of fearful facial expressions was significantly faster after anodal right/cathodal left stimulation with respect to anodal left/cathodal right and sham stimulations. In the visual perspective taking task, instead, anodal right/cathodal left stimulation negatively affected both male and female participants’ tendency to adopt another’s point of view. These findings demonstrated that concurrent facilitation of right and inhibition of left lateral prefrontal cortex can speed-up males’ responses to threatening faces whereas it interferes with the ability to adopt another’s viewpoint independently from gender. Thus, stimulation of cognitive control areas can lead to different effects on social cognitive skills depending on the affective vs. cognitive nature of the task, and on the gender-related differences in neural organization of emotion processing.     

Differential Contributions of Dorso-Ventral and Rostro-Caudal Prefrontal White Matter Tracts to Cognitive Control in Healthy Older Adults

Prefrontal cortex mediates cognitive control by means of circuitry organized along dorso-ventral and rostro-caudal axes. Along the dorso-ventral axis, ventrolateral PFC controls semantic information, whereas dorsolateral PFC encodes task rules. Along the rostro-caudal axis, anterior prefrontal cortex encodes complex rules and relationships between stimuli, whereas posterior prefrontal cortex encodes simple relationships between stimuli and behavior. Evidence of these gradients of prefrontal cortex organization has been well documented in fMRI studies, but their functional correlates have not been examined with regard to integrity of underlying white matter tracts. We hypothesized that (a) the integrity of specific white matter tracts is related to cognitive functioning in a manner consistent with the dorso-ventral and rostro-caudal organization of the prefrontal cortex, and (b) this would be particularly evident in healthy older adults. We assessed three cognitive processes that recruit the prefrontal cortex and can distinguish white matter tracts along the dorso-ventral and rostro-caudal dimensions –episodic memory, working memory, and reasoning. Correlations between cognition and fractional anisotropy as well as fiber tractography revealed: (a) Episodic memory was related to ventral prefrontal cortex-thalamo-hippocampal fiber integrity; (b) Working memory was related to integrity of corpus callosum body fibers subserving dorsolateral prefrontal cortex; and (c) Reasoning was related to integrity of corpus callosum body fibers subserving rostral and caudal dorsolateral prefrontal cortex. These findings confirm the ventrolateral prefrontal cortex''s role in semantic control and the dorsolateral prefrontal cortex''s role in rule-based processing, in accordance with the dorso-ventral prefrontal cortex gradient. Reasoning-related rostral and caudal superior frontal white matter may facilitate different levels of task rule complexity. This study is the first to demonstrate dorso-ventral and rostro-caudal prefrontal cortex processing gradients in white matter integrity.     

Representational switching by dynamical reorganization of attractor structure in a network model of the prefrontal cortex

The prefrontal cortex (PFC) plays a crucial role in flexible cognitive behavior by representing task relevant information with its working memory. The working memory with sustained neural activity is described as a neural dynamical system composed of multiple attractors, each attractor of which corresponds to an active state of a cell assembly, representing a fragment of information. Recent studies have revealed that the PFC not only represents multiple sets of information but also switches multiple representations and transforms a set of information to another set depending on a given task context. This representational switching between different sets of information is possibly generated endogenously by flexible network dynamics but details of underlying mechanisms are unclear. Here we propose a dynamically reorganizable attractor network model based on certain internal changes in synaptic connectivity, or short-term plasticity. We construct a network model based on a spiking neuron model with dynamical synapses, which can qualitatively reproduce experimentally demonstrated representational switching in the PFC when a monkey was performing a goal-oriented action-planning task. The model holds multiple sets of information that are required for action planning before and after representational switching by reconfiguration of functional cell assemblies. Furthermore, we analyzed population dynamics of this model with a mean field model and show that the changes in cell assemblies' configuration correspond to those in attractor structure that can be viewed as a bifurcation process of the dynamical system. This dynamical reorganization of a neural network could be a key to uncovering the mechanism of flexible information processing in the PFC.     

The cost of cortical computation

Electrophysiological recordings show that individual neurons in cortex are strongly activated when engaged in appropriate tasks, but they tell us little about how many neurons might be engaged by a task, which is important to know if we are to understand how cortex encodes information. For human cortex, I estimate the cost of individual spikes, then, from the known energy consumption of cortex, I establish how many neurons can be active concurrently. The cost of a single spike is high, and this severely limits, possibly to fewer than 1%, the number of neurons that can be substantially active concurrently. The high cost of spikes requires the brain not only to use representational codes that rely on very few active neurons, but also to allocate its energy resources flexibly among cortical regions according to task demand. The latter constraint explains the investment in local control of hemodynamics, exploited by functional magnetic resonance imaging, and the need for mechanisms of selective attention.     

Task-specific effects of tDCS-induced cortical excitability changes on cognitive and motor sequence set shifting performance

In this study, we tested the effects of transcranial Direct Current Stimulation (tDCS) on two set shifting tasks. Set shifting ability is defined as the capacity to switch between mental sets or actions and requires the activation of a distributed neural network. Thirty healthy subjects (fifteen per site) received anodal, cathodal and sham stimulation of the dorsolateral prefrontal cortex (DLPFC) or the primary motor cortex (M1). We measured set shifting in both cognitive and motor tasks. The results show that both anodal and cathodal single session tDCS can modulate cognitive and motor tasks. However, an interaction was found between task and type of stimulation as anodal tDCS of DLPFC and M1 was found to increase performance in the cognitive task, while cathodal tDCS of DLPFC and M1 had the opposite effect on the motor task. Additionally, tDCS effects seem to be most evident on the speed of changing sets, rather than on reducing the number of errors or increasing the efficacy of irrelevant set filtering.     

Developmental maturation of dynamic causal control signals in higher-order cognition: a neurocognitive network model

Cognitive skills undergo protracted developmental changes resulting in proficiencies that are a hallmark of human cognition. One skill that develops over time is the ability to problem solve, which in turn relies on cognitive control and attention abilities. Here we use a novel multimodal neurocognitive network-based approach combining task-related fMRI, resting-state fMRI and diffusion tensor imaging (DTI) to investigate the maturation of control processes underlying problem solving skills in 7-9 year-old children. Our analysis focused on two key neurocognitive networks implicated in a wide range of cognitive tasks including control: the insula-cingulate salience network, anchored in anterior insula (AI), ventrolateral prefrontal cortex and anterior cingulate cortex, and the fronto-parietal central executive network, anchored in dorsolateral prefrontal cortex and posterior parietal cortex (PPC). We found that, by age 9, the AI node of the salience network is a major causal hub initiating control signals during problem solving. Critically, despite stronger AI activation, the strength of causal regulatory influences from AI to the PPC node of the central executive network was significantly weaker and contributed to lower levels of behavioral performance in children compared to adults. These results were validated using two different analytic methods for estimating causal interactions in fMRI data. In parallel, DTI-based tractography revealed weaker AI-PPC structural connectivity in children. Our findings point to a crucial role of AI connectivity, and its causal cross-network influences, in the maturation of dynamic top-down control signals underlying cognitive development. Overall, our study demonstrates how a unified neurocognitive network model when combined with multimodal imaging enhances our ability to generalize beyond individual task-activated foci and provides a common framework for elucidating key features of brain and cognitive development. The quantitative approach developed is likely to be useful in investigating neurodevelopmental disorders, in which control processes are impaired, such as autism and ADHD.     

Anterior cingulate and posterior parietal cortices are sensitive to dissociable forms of conflict in a task-switching paradigm

The conflict-monitoring hypothesis posits that anterior cingulate cortex (ACC) monitors conflict in information processing and recruits dorsolateral prefrontal cortex (DLPFC) to resolve competition as needed. We used fMRI to test this prediction directly in the context of a task-switching paradigm, in which subjects responded to the color or the motion of a visual stimulus. Conflict was indexed in terms of the product of activities in areas specialized for color or motion processing on a trial-by-trial basis. Here, we report that ACC and posterior parietal cortex (PPC) were sensitive to distinct forms of conflict, at the level of the response and the stimulus representation, respectively. Activity in PPC preceded increased activity in DLPFC and predicted enhanced behavioral performance on subsequent trials. These findings suggest that ACC and PPC may act in concert to detect dissociable forms of conflict and signal to DLPFC the need for increased control.     

Stress-Induced Impairment of a Working Memory Task: Role of Spiking Rate and Spiking History Predicted Discharge

Stress, pervasive in society, contributes to over half of all work place accidents a year and over time can contribute to a variety of psychiatric disorders including depression, schizophrenia, and post-traumatic stress disorder. Stress impairs higher cognitive processes, dependent on the prefrontal cortex (PFC) and that involve maintenance and integration of information over extended periods, including working memory and attention. Substantial evidence has demonstrated a relationship between patterns of PFC neuron spiking activity (action-potential discharge) and components of delayed-response tasks used to probe PFC-dependent cognitive function in rats and monkeys. During delay periods of these tasks, persistent spiking activity is posited to be essential for the maintenance of information for working memory and attention. However, the degree to which stress-induced impairment in PFC-dependent cognition involves changes in task-related spiking rates or the ability for PFC neurons to retain information over time remains unknown. In the current study, spiking activity was recorded from the medial PFC of rats performing a delayed-response task of working memory during acute noise stress (93 db). Spike history-predicted discharge (SHPD) for PFC neurons was quantified as a measure of the degree to which ongoing neuronal discharge can be predicted by past spiking activity and reflects the degree to which past information is retained by these neurons over time. We found that PFC neuron discharge is predicted by their past spiking patterns for nearly one second. Acute stress impaired SHPD, selectively during delay intervals of the task, and simultaneously impaired task performance. Despite the reduction in delay-related SHPD, stress increased delay-related spiking rates. These findings suggest that neural codes utilizing SHPD within PFC networks likely reflects an additional important neurophysiological mechanism for maintenance of past information over time. Stress-related impairment of this mechanism is posited to contribute to the cognition-impairing actions of stress.