Specific Roles of NMDA and AMPA Receptors in Direction-Selective and Spatial Phase-Selective Responses in Visual Cortex

Rivadulla, Casto; Sharma, Jitendra; Sur, Mriganka

doi:10.1523/jneurosci.21-05-01710.2001

Cited by 49 publications

(40 citation statements)

References 50 publications

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“…A previous study in anesthetized cats (23) supported the different roles of these glutamate receptors by showing that activation of AMPA-Rs added a relatively constant number of spikes to the firing rate of a neuron, whereas activation of the NMDA-R caused an increase in response gain. Similarly, a study on direction selectivity (43) showed that AMPA-R activity produces directionally selective responses, whereas NMDA-R activity amplifies neuronal responses evoked by a stimulus moving in the preferred direction. In other words, NMDA-Rs increase the firing rate of active cells and have little effect on neurons not driven by the visual stimulus.…”

Section: Discussionmentioning

confidence: 95%

Different glutamate receptors convey feedforward and recurrent processing in macaque V1

Self

Kooijmans²,

Supèr³

et al. 2012

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

165

179

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Neurons in the primary visual cortex (V1) receive feedforward input from the thalamus, which shapes receptive-field properties. They additionally receive recurrent inputs via horizontal connections within V1 and feedback from higher visual areas that are thought to be important for conscious visual perception. Here, we investigated what roles different glutamate receptors play in conveying feedforward and recurrent inputs in macaque V1. As a measure of recurrent processing, we used figure-ground modulation (FGM), the increased activity of neurons representing figures compared with background, which depends on feedback from higher areas. We found that feedforward-driven activity was strongly reduced by the AMPA receptor antagonist 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX), whereas this drug had no effect on FGM. In contrast, blockers of the NMDA receptor reduced FGM, whereas their effect on visually driven activity varied with the subunit specificity of the drug. The NMDA receptor blocker 2-amino-5-phosphonovalerate (APV) caused a slight reduction of the visual response, whereas ifenprodil, which targets NMDA receptors containing the NMDA receptor NR2B subunit, increased the visual response. These findings demonstrate that glutamate receptors contribute differently to feedforward and recurrent processing in V1 and suggest ways to selectively disrupt recurrent processing so that its role in visual perception can be elucidated.T he areas of the primate visual cortex are arranged in a hierarchy, with feedforward connections propagating information from lower to higher areas and feedback connections carrying information in the opposite direction, back to the lower areas (1). Feedforward and recurrent processing differ greatly in function. Feedforward connections drive neurons in the visual cortex. They shape the receptive field of neurons, causing the rapid formation of tuning properties such as orientation and direction selectivity (2) and even sensitivity to complex objects such as faces. In contrast, recurrent input, carried by feedback connections from higher areas and by horizontal connections within a visual area, is thought not to drive neurons but to mediate modulatory, contextual effects (3, 4). Recurrent connections have been suggested to be involved in attention (5-7), figure-ground segregation (8-11), and conscious visual perception (12, 13), although their precise function is not well understood. One problem in studying the role of recurrent connections has been the lack of a tool to selectively inhibit them without disrupting feedforward processing. Some studies blocked the source of recurrent processing by suppressing activity in higher-level visual areas using cooling or injections of GABA while recording in lower-level areas (9,14,15). The results of these studies vary because some showed strong effects on V1 activity (15) and a decrease in contextual modulation (9), whereas others showed no effect (14). The exact effect of recurrent input into V1, therefore, remains to be elucidated.Why might feed...

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Section: Discussionmentioning

confidence: 95%

Different glutamate receptors convey feedforward and recurrent processing in macaque V1

Self

Kooijmans²,

Supèr³

et al. 2012

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

165

179

View full text Add to dashboard Cite

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“…2 also illustrates that we use slow excitation in the synapses between cortical cells (see temporal coupling profiles). The total excitatory postsynaptic potential was the sum of an ␣-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) component and a N-methyl-D-aspartate (NMDA) component (27) with equal weight integrated over time. We found that, in networks where the cortical coupling is mediated only by AMPA, the strong cortical amplification led to large-amplitude global oscillations.…”

Section: Resultsmentioning

confidence: 99%

An egalitarian network model for the emergence of simple and complex cells in visual cortex

Tao

Shelley²,

McLaughlin³

et al. 2003

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

129

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We explain how simple and complex cells arise in a large-scale neuronal network model of the primary visual cortex of the macaque. Our model consists of Ϸ4,000 integrate-and-fire, conductance-based point neurons, representing the cells in a small, 1-mm 2 patch of an input layer of the primary visual cortex. In the model the local connections are isotropic and nonspecific, and convergent input from the lateral geniculate nucleus confers cortical cells with orientation and spatial phase preference. The balance between lateral connections and lateral geniculate nucleus drive determines whether individual neurons in this recurrent circuit are simple or complex. The model reproduces qualitatively the experimentally observed distributions of both extracellular and intracellular measures of simple and complex response. Simple and complex cells may have different tasks in visual perception. Cortical cells must represent spatial properties such as surface brightness and color and the perceptual spatial organization of a scene that is the basis of form. Simple cells are necessary for all of these functions because they are the visual cortical neurons that are able to respond monotonically to signed edge contrast. Complex cells, being insensitive to spatial phase, cannot provide a cortical representation of signed contrast, but they are sensitive to texture, firing at elevated rates in response to stimuli within their receptive fields.Although long-standing and with functional implications, the simple͞complex classification is hardly sharp. Recent work by Ringach et al. (2) analyzes the extracellular responses of neurons across many experiments in macaque V1. They find that many V1 cells are neither wholly simple nor wholly complex but lie somewhere in between. And although most cells in V1 might be classified as complex, the cortical layer that receives the bulk of lateral geniculate nucleus (LGN) excitation, 4C, has simple and complex cells in approximately equal proportion.Associated with the simple͞complex classification is the influential hierarchical model of Hubel and Wiesel (1), shown schematically in Fig. 1a, wherein simple cells receive geniculate drive and the pooling of their phase-specific outputs drives the phase invariant responses of complex cells. As we argue in Results, this conception seems difficult to reconcile with recent experimental evidence. Chance, Nelson, and Abbott (3) have put forward a very different model that investigates the possible role of recurrent excitation in creating complex cells. In their model, the phase-specific outputs of excitatory simple cells drive cells coupled together in an excitatory recurrent network (Fig. 1b). Realizing this architecture by using a rate model for network activity, they find phase invariant, complex responses when recurrent excitation in the network dominates that of the simple cell inputs.Here, we study a large-scale model of the neuronal dynamics in layer 4C␣ of macaque V1, whose architecture is known better than for almost any other cortical area. Ou...

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“…LGN/V1). Within V1, other NMDA-dependent processes, such as delayed GABAergic feedback, may also contribute to neuronal motion sensitivity (Rivadulla et al, 2001). Motion sensitivity deficits, as well as more general magnocellular dysfunction Kwon et al, 1991Kwon et al, , 1992, therefore may both be manifestations of proposed disturbances in glutamatergic and/or NMDA-dependent neurotransmission in schizophrenia.…”

Section: Discussionmentioning

confidence: 99%

Magnocellular contributions to impaired motion processing in schizophrenia

Kim

Wylie

Pasternak

et al. 2006

Schizophrenia Research

133

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Patients with schizophrenia show impairments in motion processing, along with deficits in lower level processing primarily involving the magnocellular visual pathway. The present study investigates potential magnocellular contributions to impaired motion processing in schizophrenia using a combined neurophysiological and behavioral approach. As compared to prior motion studies in schizophrenia, thresholds were determined for both incoherent and coherent visual motion. In this study, velocity discrimination thresholds were measured for schizophrenia patients (n = 14) and agematched normal control subjects (n = 16) using a staircase procedure. Early visual processing was evaluated using steady-state visual evoked potentials (ssVEP), with stimuli biased toward activation of either the magnocellular or parvocellular visual pathways through luminance contrast manipulation. Patients with schizophrenia showed poor velocity discrimination for both incoherent and coherent motion, with no significant group × task interaction. Further, when coherent motion performance was measured at individually determined incoherent motion thresholds, accuracy levels for patients were similar to controls, also indicating similarity of deficit for incoherent vs. coherent motion discrimination. Impairments in velocity discrimination correlated significantly with reduced amplitude of ssVEP elicited by magnocellular -but not parvocellular -selective stimuli. This study demonstrates that deficits in motion processing in schizophrenia are significantly related to reduced activation of the magnocellular visual system. Further, this study supports and extends prior reports of impaired motion processing in schizophrenia, and indicates significant bottom-up contributions to higher-order cognitive impairments.

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Specific Roles of NMDA and AMPA Receptors in Direction-Selective and Spatial Phase-Selective Responses in Visual Cortex

Cited by 49 publications

References 50 publications

Different glutamate receptors convey feedforward and recurrent processing in macaque V1

Different glutamate receptors convey feedforward and recurrent processing in macaque V1

An egalitarian network model for the emergence of simple and complex cells in visual cortex

Magnocellular contributions to impaired motion processing in schizophrenia

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