Fiebelkorn, I. C., & Kastner, S. (2019). A Rhythmic Theory of Attention. Trends in Cognitive Science. Publisher's VersionAbstract
Recent evidence has demonstrated that environmental sampling is a fundamentally rhythmic process. Both perceptual sensitivity during covert spatial attention and the probability of overt exploratory movements are tethered to theta-band activity (3–8 Hz) in the attention network. The fronto-parietal part of this network is positioned at the nexus of sensory and motor functions, directing two tightly coupled processes related to environmental exploration: preferential routing of sensory input and saccadic eye movements. We propose that intrinsic theta rhythms temporally resolve potential functional conflicts by periodically reweighting functional connections between higher-order brain regions and either sensory or motor regions. This rhythmic reweighting alternately promotes either sampling at a behaviorally relevant location (i.e., sensory functions) or shifting to another location (i.e., motor functions).
Fiebelkorn, I. C., Pinsk, M. A., & Kastner, S. (2019). The mediodorsal pulvinar coordinates the macaque fronto-parietal network during rhythmic spatial attention. Nature Communications. Publisher's VersionAbstract
Spatial attention is discontinuous, sampling behaviorally relevant locations in theta-rhythmic cycles (3–6 Hz). Underlying this rhythmic sampling are intrinsic theta oscillations in frontal and parietal cortices that provide a clocking mechanism for two alternating attentional states that are associated with either engagement at the presently attended location (and enhanced perceptual sensitivity) or disengagement (and diminished perceptual sensitivity). It has remained unclear, however, how these theta-dependent states are coordinated across the large-scale network that directs spatial attention. The pulvinar is a candidate for such coordination, having been previously shown to regulate cortical activity. Here, we examined pulvino-cortical interactions during theta-rhythmic sampling by simultaneously recording from macaque frontal eye fields (FEF), lateral intraparietal area (LIP), and pulvinar. Neural activity propagated from pulvinar to cortex during periods of engagement, and from cortex to pulvinar during periods of disengagement. A rhythmic reweighting of pulvino-cortical interactions thus defines functional dissociations in the attention network.
Kim, N. Y., & Kastner, S. (2019). A biased competition theory for the developmental cognitive neuroscience of visuo-spatial attention. Current Opinion in Psychology , 29, 219-228. Publisher's VersionAbstract
Selective attention is crucial for navigating natural visual environments, which are often crowded with too many objects to process simultaneously. Research over the past few decades has led to influential theories describing neural mechanisms underlying selective attention in the adult brain. However, how children come to achieve adult-level selective attention functions has been explored much less. Here, we discuss specifically the existing literature on visuo-spatial attention development based on a theoretical framework that is grounded in biased competition theory, while integrating more recent evidence from neuroimaging and electrophysiology. In this forward-looking review, we emphasize that selective attention functions operate through interactions between the developing sensory cortices and fronto-parietal control network. Our framework may prove useful in probing selective attention functions in typical and atypical development.
Martin, A. B., Yang, X., Saalmann, Y. B., Wang, L., Shestyuk, A., Lin, J. J., Parvizi, J., et al. (2019). Temporal Dynamics and Response Modulation across the Human Visual System in a Spatial Attention Task: An ECoG Study. Journal of Neuroscience , 39 (2), 333-352. Publisher's VersionAbstract
The selection of behaviorally relevant information from cluttered visual scenes (often referred to as “attention”) is mediated by a cortical large-scale network consisting of areas in occipital, temporal, parietal, and frontal cortex that is organized into a functional hierarchy of feedforward and feedback pathways. In the human brain, little is known about the temporal dynamics of attentional processing from studies at the mesoscopic level of electrocorticography (ECoG), that combines millisecond temporal resolution with precise anatomical localization of recording sites. We analyzed high-frequency broadband responses (HFB) responses from 626 electrodes implanted in 8 epilepsy patients who performed a spatial attention task. Electrode locations were reconstructed using a probabilistic atlas of the human visual system. HFB responses showed high spatial selectivity and tuning, constituting ECoG response fields (RFs), within and outside the topographic visual system. In accordance with monkey physiology studies, both RF widths and onset latencies increased systematically across the visual processing hierarchy. We used the spatial specificity of HFB responses to quantitatively study spatial attention effects and their temporal dynamics to probe a hierarchical top-down model suggesting that feedback signals back propagate the visual processing hierarchy. Consistent with such a model, the strengths of attentional modulation were found to be greater and modulation latencies to be shorter in posterior parietal cortex, middle temporal cortex and ventral extrastriate cortex compared with early visual cortex. However, inconsistent with such a model, attention effects were weaker and more delayed in anterior parietal and frontal cortex.
Fiebelkorn, I. C., & Kastner, S. (2018). The Puzzling Pulvinar. Neuron.
Arcaro, M. J., Pinsk, M. A., Chen, J., & Kastner, S. (2018). Organizing principles of pulvino-cortical functional coupling in humans. Nature Communications , 9 (5382). Publisher's VersionAbstract
The pulvinar influences communication between cortical areas. We use fMRI to characterize the functional organization of the human pulvinar and its coupling with cortex. The ventral pulvinar is sensitive to spatial position and moment-to-moment transitions in visual statistics, but also differentiates visual categories such as faces and scenes. The dorsal pulvinar is modulated by spatial attention and is sensitive to the temporal structure of visual input. Cortical areas are functionally coupled with discrete pulvinar regions. The spatial organization of this coupling reflects the functional specializations and anatomical distances between cortical areas. The ventral pulvinar is functionally coupled with occipital-temporal cortices. The dorsal pulvinar is functionally coupled with frontal, parietal, and cingulate cortices, including the attention, default mode, and human-specific tool networks. These differences mirror the principles governing cortical organization of dorsal and ventral cortical visual streams. These results provide a functional framework for how the pulvinar facilitates and regulates cortical processing.
Helfrich, R. F., Fiebelkorn, I. C., Szczepanski, S. M., Lin, J. J., Parvizi, J., Knight, R. T., & Kastner, S. (2018). Neural Mechanisms of Sustained Attention Are Rhythmic. Neuron , 99 (4), 854-865.Abstract
Classic models of attention suggest that sustained neural firing constitutes a neural correlate of sustained attention. However, recent evidence indicates that behavioral performance fluctuates over time, exhibiting temporal dynamics that closely resemble the spectral features of ongoing, oscillatory brain activity. Therefore, it has been proposed that periodic neuronal excitability fluctuations might shape attentional allocation and overt behavior. However, empirical evidence to support this notion is sparse. Here, we address this issue by examining data from large-scale subdural recordings, using two different attention tasks that track perceptual ability at high temporal resolution. Our results reveal that perceptual outcome varies as a function of the theta phase even in states of sustained spatial attention. These effects were robust at the single-subject level, suggesting that rhythmic perceptual sampling is an inherent property of the frontoparietal attention network. Collectively, these findings support the notion that the functional architecture of top-down attention is intrinsically rhythmic.
Milham, M., Ai, L., Koo, B., Xu, T., Balezeau, F., Baxter, M. G., Croxson, P. L., et al. (2018). An Open Resource for Non-human Primate Imaging. Neuron , 100, 61-74. Publisher's VersionAbstract
Non-human primate neuroimaging is a rapidly growing area of research that promises to transform and scale translational and cross-species comparative neuroscience. Unfortunately, the technological and methodological advances of the past two decades have outpaced the accrual of data, which is particularly challenging given the relatively few centers that have the necessary facilities and capabilities. The PRIMatE Data Exchange (PRIME-DE) addresses this challenge by aggregating independently acquired non-human primate magnetic resonance imaging (MRI) datasets and openly sharing them via the International Neuroimaging Data-sharing Initiative (INDI). Here, we present the rationale, design, and procedures for the PRIME-DE consortium, as well as the initial release, consisting of 25 independent data collections aggregated across 22 sites (total = 217 non-human primates). We also outline the unique pitfalls and challenges that should be considered in the analysis of non-human primate MRI datasets, including providing automated quality assessment of the contributed datasets.
Fiebelkorn, I. C., Pinsk, M. A., & Kastner, S. (2018). A dynamic interplay within the frontoparietal network underlies rhythmic spatial attention. Neuron , 99, 842-53. Publisher's VersionAbstract
Classic studies of spatial attention assumed that its neural and behavioral effects were continuous over time. Recent behavioral studies have instead revealed that spatial attention leads to alternating periods of heightened or diminished perceptual sensitivity. Yet, the neural basis of these rhythmic fluctuations has remained largely unknown. We show that a dynamic interplay within the macaque frontoparietal network accounts for the rhythmic properties of spatial attention. Neural oscillations characterize functional interactions between the frontal eye fields (FEF) and the lateral intraparietal area (LIP), with theta phase (3–8 Hz) coordinating two rhythmically alternating states. The first is defined by FEF-dominated beta-band activity, associated with suppressed attentional shifts, and LIP-dominated gamma-band activity, associated with enhanced visual processing and better behavioral performance. The second is defined by LIP-specific alpha-band activity, associated with attenuated visual processing and worse behavioral performance. Our findings reveal how network-level interactions organize environmental sampling into rhythmic cycles.
Parvizi, J., & Kastner, S. (2018). Promises and limitations of human intracranial electroencephalography. Nature Neuroscience , 21, 474-483.Abstract
Intracranial electroencephalography (iEEG), also known as electrocorticography when using subdural grid electrodes or stereotactic EEG when using depth electrodes, is blossoming in various fields of human neuroscience. In this article, we highlight the potentials of iEEG in exploring functions of the human brain while also considering its limitations. The iEEG signal provides anatomically precise information about the selective engagement of neuronal populations at the millimeter scale and the temporal dynamics of their engagement at the millisecond scale. If several nodes of a given network are monitored simultaneously with implanted electrodes, the iEEG signals can also reveal information about functional interactions within and across networks during different stages of neural computation. As such, human iEEG can complement other methods of neuroscience beyond simply replicating what is already known, or can be known, from noninvasive lines of research in humans or from invasive recordings in nonhuman mammalian brains.
Halassa, M. M., & Kastner, S. (2017). Thalamic functions in distributed cognitive control. Nature Neuroscience , 20, 1669-1679.Abstract
Cognition can be conceptualized as a set of algorithmic control functions whose real-time deployment determines how an organism stores and uses information to guide thought and action. A subset of these functions is required for goal-directed selection and amplification of sensory signals-broadly referred to as attention-and for its flexible control and its interaction with processes such as working memory and decision making. While the contribution of recurrent cortical microcircuits to cognition has been extensively studied, the role of the thalamus is just beginning to be elucidated. Here we highlight recent studies across rodents and primates showing how thalamus contributes to attentional control. In addition to high-fidelity information relay to or between cortical regions, thalamic circuits shift and sustain functional interactions within and across cortical areas. This thalamic process enables rapid coordination of spatially segregated cortical computations, thereby constructing task-relevant functional networks. Because such function may be critical for cognitive flexibility, clarifying its mechanisms will likely expand our basic understanding of cognitive control and its perturbation in disease.
Kastner, S., Chen, Q., Jeong, S. K., & Mruczek, R. E. B. (2017). A brief comparative review of primate posterior parietal cortex: A novel hypothesis on the human toolmaker. Neuropsychologia , 105, 123-34.Abstract
The primate visual system contains two major cortical pathways: a ventral-temporal pathway that has been associated with object processing and recognition, and a dorsal-parietal pathway that has been associated with spatial processing and action guidance. Our understanding of the role of the dorsal pathway, in particular, has greatly evolved within the framework of the two-pathway hypothesis since its original conception. Here, we present a comparative review of the primate dorsal pathway in humans and monkeys based on electrophysiological, neuroimaging, neuropsychological, and neuroanatomical studies. We consider similarities and differences across species in terms of the topographic representation of visual space; specificity for eye, reaching, or grasping movements; multi-modal response properties; and the representation of objects and tools. We also review the relative anatomical location of functionally- and topographically-defined regions of the posterior parietal cortex. An emerging theme from this comparative analysis is that non-spatial information is represented to a greater degree, and with increased complexity, in the human dorsal visual system. We propose that non-spatial information in the primate parietal cortex contributes to the perception-to-action system aimed at manipulating objects in peripersonal space. In humans, this network has expanded in multiple ways, including the development of a dorsal object vision system mirroring the complexity of the ventral stream, the integration of object information with parietal working memory systems, and the emergence of tool-specific object representations in the anterior intraparietal sulcus and regions of the inferior parietal lobe. We propose that these evolutionary changes have enabled the emergence of human-specific behaviors, such as the sophisticated use of tools.
Kastner, S., & Knight, R. T. (2017). Bringing Kids into the Scientific Review Process. Neuron , 93, 12-14.Abstract
Frontiers for Young Minds puts kids in charge of scientific publications by having them control the review process. This provides kids the ability to shape the way science is taught and to better understand the scientific method.
Bonnefond, M., Kastner, S., & Jensen, O. (2017). Communication between Brain Areas Based on Nested Oscillations. eNeuro , 4.Abstract
Unraveling how brain regions communicate is crucial for understanding how the brain processes external and internal information. Neuronal oscillations within and across brain regions have been proposed to play a crucial role in this process. Two main hypotheses have been suggested for routing of information based on oscillations, namely communication through coherence and gating by inhibition. Here, we propose a framework unifying these two hypotheses that is based on recent empirical findings. We discuss a theory in which communication between two regions is established by phase synchronization of oscillations at lower frequencies (<25 Hz), which serve as temporal reference frame for information carried by high-frequency activity (>40 Hz). Our framework, consistent with numerous recent empirical findings, posits that cross-frequency interactions are essential for understanding how large-scale cognitive and perceptual networks operate.
Popov, T., Kastner, S., & Jensen, O. (2017). FEF-Controlled Alpha Delay Activity Precedes Stimulus-Induced Gamma-Band Activity in Visual Cortex. J Neurosci , 37, 4117-4127.Abstract
Recent findings in the visual system of nonhuman primates have demonstrated an important role of gamma-band activity (40-100 Hz) in the feedforward flow of sensory information, whereas feedback control appears to be established dynamically by oscillations in the alpha (8-13 Hz) and beta (13-18 Hz) bands (van Kerkoerle et al., 2014; Bastos et al., 2015). It is not clear, however, how alpha oscillations are controlled and how they interact with the flow of visual information mediated by gamma-band activity. Using noninvasive human MEG recordings in subjects performing a visuospatial attention task, we show that fluctuations in alpha power during a delay period in a spatial attention task preceded subsequent stimulus-driven gamma-band activity. Importantly, these interactions correlated with behavioral performance. Using Granger analysis, we further show that the right frontal-eye field (rFEF) exerted feedback control of the visual alpha oscillations. Our findings suggest that alpha oscillations controlled by the FEF route cortical information flow by modulating gamma-band activity.SIGNIFICANCE STATEMENT Visual perception relies on a feedforward flow of information from sensory regions, which is modulated by a feedback drive. We have identified the neuronal dynamics supporting integration of the feedforward and feedback information. Alpha oscillations in early visual regions reflect feedback control when spatial attention is allocated and this control is exercised by the right frontal eye field. Importantly, the alpha-band activity predicted both performance and activity in the gamma band. In particular, gamma activity was modulated by the phase of the alpha oscillations. These findings provide novel insight into how the brain operates as a network and suggest that the integration of feedforward and feedback information is implemented by cross-frequency interactions between slow and fast neuronal oscillations.
Kaster, S., & Knight, R. T. (2016). Bringing Kids into the Scientific Review Process. Neuron , 93 (1).Abstract
Frontiers for Young Minds puts kids in charge of scientific publications by having them control the review process. This provides kids the ability to shape the way science is taught and to better understand the scientific method.
Keane, B. P., Paterno, D., Kastner, S., & Silverstein, S. M. (2016). Visual integration dysfunction in schizophrenia arises by the first psychotic episode and worsens with illness duration. J Abnorm Psychol , 125, 543-9.Abstract
Visual integration dysfunction characterizes schizophrenia, but prior studies have not yet established whether the problem arises by the first psychotic episode or worsens with illness duration. To investigate the issue, we compared chronic schizophrenia patients (SZs), first episode psychosis patients (FEs), and well-matched healthy controls on a brief but sensitive psychophysical task in which subjects attempted to locate an integrated shape embedded in noise. Task difficulty depended on the number of noise elements co-presented with the shape. For half of the experiment, the entire display was scaled down in size to produce a high spatial frequency (HSF) condition, which has been shown to worsen patient integration deficits. Catch trials-in which the circular target appeared without noise-were also added so as to confirm that subjects were paying adequate attention. We found that controls integrated contours under noisier conditions than FEs, who, in turn, integrated better than SZs. These differences, which were at times large in magnitude (d = 1.7), clearly emerged only for HSF displays. Catch trial accuracy was above 95% for each group and could not explain the foregoing differences. Prolonged illness duration predicted poorer HSF integration across patients, but age had little effect on controls, indicating that the former factor was driving the effect in patients. Taken together, a brief psychophysical task efficiently demonstrates large visual integration impairments in schizophrenia. The deficit arises by the first psychotic episode, worsens with illness duration, and may serve as a biomarker of illness progression. (PsycINFO Database Record
Wang, L., Mruczek, R. E. B., Arcaro, M. J., & Kastner, S. (2015). Probabilistic Maps of Visual Topography in Human Cortex. Cereb Cortex , 25, 3911-31.Abstract
The human visual system contains an array of topographically organized regions. Identifying these regions in individual subjects is a powerful approach to group-level statistical analysis, but this is not always feasible. We addressed this limitation by generating probabilistic maps of visual topographic areas in 2 standardized spaces suitable for use with adult human brains. Using standard fMRI paradigms, we identified 25 topographic maps in a large population of individual subjects (N = 53) and transformed them into either a surface- or volume-based standardized space. Here, we provide a quantitative characterization of the inter-subject variability within and across visual regions, including the likelihood that a given point would be classified as a part of any region (full probability map) and the most probable region for any given point (maximum probability map). By evaluating the topographic organization across the whole of visual cortex, we provide new information about the organization of individual visual field maps and large-scale biases in visual field coverage. Finally, we validate each atlas for use with independent subjects. Overall, the probabilistic atlases quantify the variability of topographic representations in human cortex and provide a useful reference for comparing data across studies that can be transformed into these standard spaces.
Seidl-Rathkopf, K. N., Turk-Browne, N. B., & Kastner, S. (2015). Automatic guidance of attention during real-world visual search. Atten Percept Psychophys , 77, 1881-95.Abstract
Looking for objects in cluttered natural environments is a frequent task in everyday life. This process can be difficult, because the features, locations, and times of appearance of relevant objects often are not known in advance. Thus, a mechanism by which attention is automatically biased toward information that is potentially relevant may be helpful. We tested for such a mechanism across five experiments by engaging participants in real-world visual search and then assessing attentional capture for information that was related to the search set but was otherwise irrelevant. Isolated objects captured attention while preparing to search for objects from the same category embedded in a scene, as revealed by lower detection performance (Experiment 1A). This capture effect was driven by a central processing bottleneck rather than the withdrawal of spatial attention (Experiment 1B), occurred automatically even in a secondary task (Experiment 2A), and reflected enhancement of matching information rather than suppression of nonmatching information (Experiment 2B). Finally, attentional capture extended to objects that were semantically associated with the target category (Experiment 3). We conclude that attention is efficiently drawn towards a wide range of information that may be relevant for an upcoming real-world visual search. This mechanism may be adaptive, allowing us to find information useful for our behavioral goals in the face of uncertainty.
Saalmann, Y. B., & Kastner, S. (2015). The cognitive thalamus. Front Syst Neurosci , 9 39.