Different glutamate receptors convey feedforward and recurrent processing in macaque V1

Self, Matthew W.; Kooijmans, Roxana N; Supèr, Hans; Lamme, Victor A. F.; Roelfsema, Pieter R.

doi:10.1073/pnas.1119527109

Cited by 160 publications

(202 citation statements)

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“…First, we applied microstimulation in one area while recording the oscillations in the other area. Second, we locally infused blockers of AMPA and NMDA receptors thought to be differentially involved in feedforward and feedback processing (24,25). All our results converged onto a straightforward conclusion: γ-oscillations in the visual cortex travel in the feedforward direction, whereas α-oscillations index feedback effects.…”

supporting

confidence: 55%

Alpha and gamma oscillations characterize feedback and feedforward processing in monkey visual cortex

Kerkoerle

Self

Dagnino

et al. 2014

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

Self Cite

846

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776

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This Feature Article is part of a series identified by the Editorial Board as reporting findings of exceptional significance.Edited by Terrence J. Sejnowski, Salk Institute for Biological Studies, La Jolla, CA, and approved August 8, 2014 (received for review February 22, 2014) Cognitive functions rely on the coordinated activity of neurons in many brain regions, but the interactions between cortical areas are not yet well understood. Here we investigated whether lowfrequency (α) and high-frequency (γ) oscillations characterize different directions of information flow in monkey visual cortex. We recorded from all layers of the primary visual cortex (V1) and found that γ-waves are initiated in input layer 4 and propagate to the deep and superficial layers of cortex, whereas α-waves propagate in the opposite direction. Simultaneous recordings from V1 and downstream area V4 confirmed that γ-and α-waves propagate in the feedforward and feedback direction, respectively. Microstimulation in V1 elicited γ-oscillations in V4, whereas microstimulation in V4 elicited α-oscillations in V1, thus providing causal evidence for the opposite propagation of these rhythms. Furthermore, blocking NMDA receptors, thought to be involved in feedback processing, suppressed α while boosting γ. These results provide new insights into the relation between brain rhythms and cognition.neuronal synchronization | attention | perceptual organization | phase coherence | Granger causality A reas of the visual cortex are arranged hierarchically, with low-level areas representing simple features and higher areas representing the more complex aspects of the visual world (1, 2). Neurons in many visual areas are coactive during the perception of a visual stimulus and it is difficult to disentangle the influences of lower areas onto higher areas from the effects that go in the opposite direction (3). Studies of visual cognition could benefit enormously from markers of cortical activity that distinguish between feedforward and feedback effects. One such putative marker is cortical oscillatory activity, because oscillations of different frequencies have been proposed to propagate either in feedforward or in the feedback direction (4, 5), but experimental evidence for this view is sparse (6).Low-frequency rhythms, like the α-rhythm-which is particularly pronounced in the visual cortex-have been proposed to characterize spontaneous activity (7,8) as the α-rhythm increases when the subject closes the eyes (9). More recent observations have also implicated α-oscillations in the active suppression of irrelevant, unattended information (10, 11). In contrast, the high-frequency γ-rhythm increases if visual stimuli are presented, and in particular if they are task-relevant (12, 13). One influential hypothesis has been that γ-oscillations play a role in feature binding (14), but later studies cast doubt on this proposal (15,16). A more recent hypothesis holds that γ-oscillations facilitate the communication between cortical areas (17), but both evidence in fa...

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supporting

confidence: 55%

Alpha and gamma oscillations characterize feedback and feedforward processing in monkey visual cortex

Kerkoerle

Self

Dagnino

et al. 2014

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

Self Cite

846

138

776

View full text Add to dashboard Cite

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“…Furthermore, contextual modulation requires the transmission of a great deal of information, and about 75% of all cortical connections are directly between pyramidal cells (Braitenberg and Schuz, 1991). Direct evidence of a role for NMDARs in contextual modulation was shown by Self et al (2012) using the well-established phenomenon of figure-ground modulation. This was almost abolished when NMDARs were blocked in V1, whereas the purely feedforward component of pyramidal cell response was largely unaffected.…”

Section: Modulation That Amplifies Responses To Rf Inputmentioning

confidence: 99%

On the functions, mechanisms, and malfunctions of intracortical contextual modulation

Phillips

Clark

Silverstein

2015

Neuroscience & Biobehavioral Reviews

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A broad neuron-centric conception of contextual modulation is reviewed and re-assessed in the light of recent neurobiological studies of amplification, suppression, and synchronization. Behavioural and computational studies of perceptual and higher cognitive functions that depend on these processes are outlined, and evidence that those functions and their neuronal mechanisms are impaired in schizophrenia is summarized. Finally, we compare and assess the long-term biological functions of contextual modulation at the level of computational theory as formalized by the theories of coherent infomax and free energy reduction. We conclude that those theories, together with the many empirical findings reviewed, show how contextual modulation at the neuronal level enables the cortex to flexibly adapt the use of its knowledge to current circumstances by amplifying and grouping relevant activities and by suppressing irrelevant activities.

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“…In support of this argument, a recent study showed that figure-ground modulation is suppressed by local injection of an NMDA antagonist into V1. 51 Given that figure-ground modulation depends on top-down signals from higher-order visual areas, 26,27 the authors suggested this effect may be due to a blockade of NMDA spikes in the apical pyramidal dendrites of V1 neurons. This would explain Anesthetics can inhibit the hyperpolarization-activated current I h , a leak conductance, which uncouples the somatic and dendritic compartments of the pyramidal cell under physiological conditions.…”

Section: The Effects Of General Anesthetics On Apical Dendrites Of Pymentioning

confidence: 99%

The Role of Dendritic Signaling in the Anesthetic Suppression of Consciousness

Meyer

2015

Anesthesiology

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Despite considerable progress in the identification of the molecular targets of general anesthetics, it remains unclear how these drugs affect the brain at the systems level to suppress consciousness. According to recent proposals, anesthetics may achieve this feat by interfering with corticocortical topdown processes, that is, by interrupting information flow from association to early sensory cortices. Such a view entails two immediate questions. First, at which anatomical site, and by virtue of which physiological mechanism, do anesthetics interfere with top-down signals? Second, why does a breakdown of top-down signaling cause unconsciousness? While an answer to the first question can be gleaned from emerging neurophysiological evidence on dendritic signaling in cortical pyramidal neurons, a response to the second is offered by increasingly popular theoretical frameworks that place the element of prediction at the heart of conscious perception. Science magazine posed this question in a special section titled "What don't we know?," dedicated to the greatest challenges of contemporary science. 1 "Scientists are chipping away at the drugs' effects on individual neurons," the article reads, "but understanding how they render us unconscious will be a tougher nut to crack." This prediction proved correct: a decade later, we have expanded considerably our knowledge of the molecular targets of general anesthetics, but it remains enigmatic how these drugs affect the brain at the systems level. Why does the potentiation of γ-aminobutyric acid (GABA) receptors caused by propofol or desflurane cause unconsciousness? How are the brain's computational processes affected by this and other molecular mechanisms of anesthetics, so that patients undergoing surgery cease to experience their surrounds in terms of sight, sound, and touch? Anesthesiologists and cognitive neuroscientists alike have been captivated by these questions and have proposed a number of models in an attempt to answer them, such as Flohr's "information processing theory of anesthesia," 2 Alkire's "thalamic consciousness switch hypothesis," 3-6 Mashour's "cognitive unbinding paradigm," 7,8 John and Prichep's "anesthetic cascade," 9 or Hudetz's "forgotten present." 10,11 We shall return to some of these frameworks in a later section of the article.One recent development is particularly intriguing. Given that the most striking feature of general anesthesia is an interruption of the patient's ability to perceive the environment, it would appear intuitive for anesthetics to interfere primarily with bottom-up information flow along the sensory pathways, that is, with the signals that carry perceptual information from the thalamus to the primary sensory cortices and on to unimodal and multimodal association cortices. However, the very opposite appears to be the case. Several recent studies-carried out in both humans and animals, and using a variety of different anesthetic agents-have investigated differences in directional corticocortical connectivity bet...

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Different glutamate receptors convey feedforward and recurrent processing in macaque V1

Cited by 160 publications

References 48 publications

Alpha and gamma oscillations characterize feedback and feedforward processing in monkey visual cortex

Alpha and gamma oscillations characterize feedback and feedforward processing in monkey visual cortex

On the functions, mechanisms, and malfunctions of intracortical contextual modulation

The Role of Dendritic Signaling in the Anesthetic Suppression of Consciousness

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