Widespread correlation patterns of fMRI signal across visual cortex reflect eccentricity organization

Arcaro, Michael; Honey, Christopher J.; Mruczek, Ryan E. B.; Kästner, Sabine; Hasson, Uri

doi:10.7554/elife.03952

Cited by 56 publications

(70 citation statements)

References 99 publications

(214 reference statements)

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“…Similar observations have been made for maps of activity across cat primary visual cortex (5,46,47), where activity patterns in the absence of visual stimulation reproduce fine-scale functional organization. Between visual areas, multiple studies have demonstrated retinotopically specific patterns of connectivity across hemispheres in both monkeys and humans (7,(9)(10)(11), and human studies have demonstrated differential connectivity within distinct visual pathways (12). Our study helps to link the fine-scale organization of intrinsic activity within areas, with that of the largescale study of coupling between areas by investigating the fine temporal and spatial dynamics of interareal coupling within the visual system.…”

Section: Discussionmentioning

confidence: 95%

Stimulus-induced visual cortical networks are recapitulated by spontaneous local and interareal synchronization

Lewis

Bosman

Womelsdorf

2016

Proc. Natl. Acad. Sci. U.S.A.

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Intrinsic covariation of brain activity has been studied across many levels of brain organization. Between visual areas, neuronal activity covaries primarily among portions with similar retinotopic selectivity. We hypothesized that spontaneous interareal coactivation is subserved by neuronal synchronization. We performed simultaneous high-density electrocorticographic recordings across the dorsal aspect of several visual areas in one hemisphere in each of two awake monkeys to investigate spatial patterns of local and interareal synchronization. We show that stimulation-induced patterns of interareal coactivation were reactivated in the absence of stimulation for the visual quadrant covered. Reactivation occurred through both interareal cofluctuation of local activity and interareal phase synchronization. Furthermore, the trial-by-trial covariance of the induced responses recapitulated the pattern of interareal coupling observed during stimulation, i.e., the signal correlation. Reactivation-related synchronization showed distinct peaks in the theta, alpha, and gamma frequency bands. During passive states, this rhythmic reactivation was augmented by specific patterns of arrhythmic correspondence. These results suggest that networks of intrinsic covariation observed at multiple levels and with several recording techniques are related to synchronization and that behavioral state may affect the structure of intrinsic dynamics.vision | intrinsic activity | oscillations | connectivity | networks A classical approach to perceptual neuroscience suggests that the brain should respond identically to repetitions of identical stimuli. In this framework, endogenously driven variance in the brain's response to repeated stimuli is considered noise (1). However, this so-called noise has been found to be highly structured and influenced by behavioral context (2). In fact, such variation is a flavor of the ongoing, spontaneous activity of the brain. Both the variation in the brain's response to identical stimuli and its spontaneous activity in the absence of stimulation are endogenously generated and structured in spatially specific intrinsic networks. Highly specific intrinsic networks have been described at essentially all spatial scales: from two individual neurons up to the whole brain. Membrane potentials of nearby neurons show a high degree of spontaneous correlation (3). Neuronal spike rates cofluctuate across physically identical trials, and this socalled noise correlation between neurons is related to the similarity in their stimulus selectivity (4). Correspondingly, when entire maps of population activity are investigated, patterns of activation induced by stimuli are found to reoccur spontaneously (5). The same holds across neighboring maps in auditory cortex, where population activity spontaneously reproduces the tonotopic organization (6). Such coactivations can also be observed with functional MRI (fMRI). In visual cortex, regions selective for either foveal or peripheral stimuli, show correlated blood-oxygen level-d...

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Section: Discussionmentioning

confidence: 95%

Stimulus-induced visual cortical networks are recapitulated by spontaneous local and interareal synchronization

Lewis

Bosman

Womelsdorf

2016

Proc. Natl. Acad. Sci. U.S.A.

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“…Despite this, the relevance of spontaneous correlations to the finer scales of organization that underlie cognitive representations has not been determined. Some aspects of finescaled organization in sensory cortex are reflected in spontaneous correlation structure, including retinotopic eccentricity biases (19) and orientation maps (20). Analyses that identify discontinuities in spontaneous correlation structure have also been applied in PFC to characterize areal boundaries (16,18).…”

Section: Discussionmentioning

confidence: 99%

“…Analyses of spontaneous correlations have been used to identify multiple large-scale functional networks (4,5,15) and boundaries between functional areas (2,(16)(17)(18) in human and nonhuman primate association cortex. The spontaneous correlation structure also mirrors established fine-scaled principles of functional organization in visual cortex, such as preferences for retinotopic position (19) and stimulus orientation (20). We therefore leveraged spontaneous activity to examine the finescaled functional organization of human PFC.…”

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confidence: 99%

Distributed representation of context by intrinsic subnetworks in prefrontal cortex

Waskom

Wagner

2017

Proc. Natl. Acad. Sci. U.S.A.

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Human prefrontal cortex supports goal-directed behavior by representing abstract information about task context. The organizational basis of these context representations, and of representations underlying other higher-order processes, is unknown. Here, we use multivariate decoding and analyses of spontaneous correlations to show that context representations are distributed across subnetworks within prefrontal cortex. Examining targeted prefrontal regions, we found that pairs of voxels with similar context preferences exhibited spontaneous correlations that were approximately twice as large as those between pairs with opposite context preferences. This subnetwork organization was stable across task-engaged and resting states, suggesting that abstract context representations are constrained by an intrinsic functional architecture. These results reveal a principle of fine-scaled functional organization in association cortex.fMRI | resting-state | rule | cognitive control | functional organization T he cerebral cortex exhibits functional organization at multiple spatial scales. At a coarse scale, the cortex is parcellated into functional areas (1, 2) that coordinate as networks through longrange connections (3-5). These areas represent and compute information with functional circuitry that is organized more finely. Some fine-scaled, intrinsic principles have been described in detail, particularly for sensory cortex (6, 7). In contrast, the subregional organization of prefrontal cortex (PFC), which gives rise to higherorder processes, including attention, decision-making, and goaldirected action (8, 9), remains largely uncharacterized. Whether PFC representations are encoded within an equipotential system or constrained by an intrinsic functional architecture is currently unknown.Sensory cortex can be mapped by parametrically varying stimulus attributes and measuring changes in the neural response, but complex and dynamic response properties limit the effectiveness of this approach for mapping PFC and other association regions. An alternate strategy is to leverage spontaneous variability in neural activity. Neural responses to repeated presentations of sensory stimuli, or in the absence of stimulation and explicit task demands, exhibit variability that is attributed to ongoing spontaneous activity (10-13). Traditional analyses consider spontaneous activity to be noise, but there is increasing evidence that shared spontaneous variability is a signature of functional organization (14). Analyses of spontaneous correlations have been used to identify multiple large-scale functional networks (4,5,15) and boundaries between functional areas (2, 16-18) in human and nonhuman primate association cortex. The spontaneous correlation structure also mirrors established fine-scaled principles of functional organization in visual cortex, such as preferences for retinotopic position (19) and stimulus orientation (20). We therefore leveraged spontaneous activity to examine the finescaled functional organization of human PFC.We focus...

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“…For example, the human visual cortex shows widely spread and highly structured spontaneous BOLD fluctuations in the absence of visual inputs (e.g., Arcaro et al, 2015;Nir et al, 2006). The structure of the spontaneous fluctuations appears to be highly informative and likely reflects the statistics of the natural environment and cognitive traits (Berkes et al, 2011;Harmelech and Malach, 2013).…”

Section: Introduction: Two Modes Of Cortical Functionmentioning

confidence: 98%

Spontaneous Fluctuations and Non-linear Ignitions: Two Dynamic Faces of Cortical Recurrent Loops

Moutard

Dehaene

Malach

2015

Neuron

100

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Recent human neurophysiological recordings have uncovered two fundamental modes of cerebral cortex activity with distinct dynamics: an active mode characterized by a rapid and sustained activity ("ignition") and a spontaneous (resting-state) mode, manifesting ultra-slow fluctuations of low amplitude. We propose that both dynamics reflect two faces of the same recurrent loop mechanism: an integration device that accumulates ongoing stochastic activity and, either spontaneously or in a task-driven manner, crosses a dynamic threshold and ignites, leading to content-specific awareness. The hypothesis can explain a rich set of behavioral and neuronal phenomena, such as perceptual threshold, the high non-linearity of visual responses, the subliminal nature of spontaneous activity fluctuations, and the slow activity buildup anticipating spontaneous behavior (e.g., readiness potential). Further elaborations of this unified scheme, such as a cascade of integrators with different ignition thresholds or multi-stable states, can account for additional complexities in the repertoire of human cortical dynamics.

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Widespread correlation patterns of fMRI signal across visual cortex reflect eccentricity organization

Cited by 56 publications

References 99 publications

Stimulus-induced visual cortical networks are recapitulated by spontaneous local and interareal synchronization

Stimulus-induced visual cortical networks are recapitulated by spontaneous local and interareal synchronization

Distributed representation of context by intrinsic subnetworks in prefrontal cortex

Spontaneous Fluctuations and Non-linear Ignitions: Two Dynamic Faces of Cortical Recurrent Loops

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