Acetylcholine Dynamically Controls Spatial Integration in Marmoset Primary Visual Cortex

Recent in vitro studies have shown that acetylcholine (ACh) selectively reduces the efficacy of lateral cortical connections via a muscarinic mechanism, while boosting the efficacy of thalamocortical/feed-forward connections via a nicotinic mechanism. This suggests that high levels of ACh should reduce center-surround interactions of neurons in primary visual cortex, making cells more reliant on feed-forward information. In line with this hypothesis, we show that local iontophoretic application of ACh in primate primary visual cortex reduced the extent of spatial integration, assessed by recording a neurons' length tuning. When ACh was externally applied, neurons' preferred length shifted toward shorter bars, showing reduced impact of the extra-classical receptive field. We fitted a difference and a ratio of Gaussian model to these data to determine the underlying mechanisms of this dynamic change of spatial integration. These models assume overlapping summation and suppression areas with different widths and gains to be responsible for spatial integration and size tuning. ACh significantly reduced the extent of the summation area, but had no significant effect on the extent of the suppression area. In line with previous studies, we also show that applying ACh enhanced the response in the majority of cells, especially in the later (sustained) part of the response. These findings are similar to effects of attention on neuronal activity. The natural release of ACh is strongly linked with states of arousal and attention. Our results may therefore be relevant to the neurobiological mechanism of attention.

Download Full-text

Faculty Opinions recommendation of Acetylcholine dynamically controls spatial integration in marmoset primary visual cortex.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1024684.290804 ◽

2005 ◽

Author(s):

John Reynolds

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Spatial Integration

Download Full-text

Dynamic Properties of Recurrent Inhibition in Primary Visual Cortex: Contrast and Orientation Dependence of Contextual Effects

Journal of Neurophysiology ◽

10.1152/jn.2000.83.2.1019 ◽

2000 ◽

Vol 83 (2) ◽

pp. 1019-1030 ◽

Cited By ~ 61

Author(s):

Valentin Dragoi ◽

Mriganka Sur

Keyword(s):

Visual Cortex ◽

Receptive Field ◽

Primary Visual Cortex ◽

Dynamic Properties ◽

Orientation Dependence ◽

Recurrent Inhibition ◽

Inhibitory Neurons ◽

Classical Receptive Field ◽

Contextual Interactions ◽

Receptive Field Center

A fundamental feature of neural circuitry in the primary visual cortex (V1) is the existence of recurrent excitatory connections between spiny neurons, recurrent inhibitory connections between smooth neurons, and local connections between excitatory and inhibitory neurons. We modeled the dynamic behavior of intermixed excitatory and inhibitory populations of cells in V1 that receive input from the classical receptive field (the receptive field center) through feedforward thalamocortical afferents, as well as input from outside the classical receptive field (the receptive field surround) via long-range intracortical connections. A counterintuitive result is that the response of oriented cells can be facilitated beyond optimal levels when the surround stimulus is cross-oriented with respect to the center and suppressed when the surround stimulus is iso-oriented. This effect is primarily due to changes in recurrent inhibition within a local circuit. Cross-oriented surround stimulation leads to a reduction of presynaptic inhibition and a supraoptimal response, whereas iso-oriented surround stimulation has the opposite effect. This mechanism is used to explain the orientation and contrast dependence of contextual interactions in primary visual cortex: responses to a center stimulus can be both strongly suppressed and supraoptimally facilitated as a function of surround orientation, and these effects diminish as stimulus contrast decreases.

Download Full-text

Contrast-Dependent Variations in the Excitatory Classical Receptive Field and Suppressive Nonclassical Receptive Field of Cat Primary Visual Cortex

Cerebral Cortex ◽

10.1093/cercor/bhs012 ◽

2012 ◽

Vol 23 (2) ◽

pp. 283-292 ◽

Cited By ~ 14

Author(s):

K. Chen ◽

X.-M. Song ◽

C.-Y. Li

Keyword(s):

Visual Cortex ◽

Receptive Field ◽

Primary Visual Cortex ◽

Classical Receptive Field

Download Full-text

A model for the estimate of local image velocity by cells in the visual cortex

Proceedings of the Royal Society of London Series B Biological Sciences ◽

10.1098/rspb.1990.0012 ◽

1990 ◽

Vol 239 (1295) ◽

pp. 129-161 ◽

Cited By ~ 129

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Frequency Tuning ◽

Temporal Frequency ◽

Spatial Integration ◽

Temporal Area ◽

Image Velocity ◽

Tuning Curves ◽

Spatio Temporal ◽

Local Image

Some computational theories of motion perception assume that the first stage en route to this perception is the local estimate of image velocity. However, this assumption is not supported by data from the primary visual cortex. Its motion sensitive cells are not selective to velocity, but rather are directionally selective and tuned to spatio-temporal frequencies. Accordingly, physiologically based theories start with filters selective to oriented spatio-temporal frequencies. This paper shows that computational and physiological theories do not necessarily conflict, because such filters may, as a population, compute velocity locally. To prove this point, we show how to combine the outputs of a class of frequency tuned filters to detect local image velocity. Furthermore, we show that the combination of filters may simulate ‘Pattern’ cells in the middle temporal area (MT), whereas each filter simulates primary visual cortex cells. These simulations include three properties of the primary cortex. First, the spatio-temporal frequency tuning curves of the individual filters display approximate space-time separability. Secondly, their direction-of-motion tuning curves depend on the distribution of orientations of the components of the Fourier decomposition and speed of the stimulus. Thirdly, the filters show facilitation and suppression for responses to apparent motions in the preferred and null directions, respectively. It is suggested that the MT’s role is not to solve the aperture problem, but to estimate velocities from primary cortex information. The spatial integration that accounts for motion coherence may be postponed to a later cortical stage.

Download Full-text

Adult Cortical Dynamics

Physiological Reviews ◽

10.1152/physrev.1998.78.2.467 ◽

1998 ◽

Vol 78 (2) ◽

pp. 467-485 ◽

Cited By ~ 248

Author(s):

CHARLES D. GILBERT

Keyword(s):

Visual Cortex ◽

Functional Properties ◽

Primary Visual Cortex ◽

Visual Information ◽

Visual Space ◽

Visual Pathway ◽

Local Features ◽

Spatial Integration ◽

Cortical Dynamics ◽

Wide Range

Gilbert, Charles D. Adult Cortical Dynamics. Physiol. Rev. 78: 467–485, 1998. — There are many influences on our perception of local features. What we see is not strictly a reflection of the physical characteristics of a scene but instead is highly dependent on the processes by which our brain attempts to interpret the scene. As a result, our percepts are shaped by the context within which local features are presented, by our previous visual experiences, operating over a wide range of time scales, and by our expectation of what is before us. The substrate for these influences is likely to be found in the lateral interactions operating within individual areas of the cerebral cortex and in the feedback from higher to lower order cortical areas. Even at early stages in the visual pathway, cells are far more flexible in their functional properties than previously thought. It had long been assumed that cells in primary visual cortex had fixed properties, passing along the product of a stereotyped operation to the next stage in the visual pathway. Any plasticity dependent on visual experience was thought to be restricted to a period early in the life of the animal, the critical period. Furthermore, the assembly of contours and surfaces into unified percepts was assumed to take place at high levels in the visual pathway, whereas the receptive fields of cells in primary visual cortex represented very small windows on the visual scene. These concepts of spatial integration and plasticity have been radically modified in the past few years. The emerging view is that even at the earliest stages in the cortical processing of visual information, cells are highly mutable in their functional properties and are capable of integrating information over a much larger part of visual space than originally believed.

Download Full-text

Unique spatial integration in mouse primary visual cortex and higher visual areas

10.1101/643007 ◽

2019 ◽

Cited By ~ 1

Author(s):

Kevin A. Murgas ◽

Ashley M. Wilson ◽

Valerie Michael ◽

Lindsey L. Glickfeld

Keyword(s):

Visual Cortex ◽

Visual System ◽

Primary Visual Cortex ◽

Spatial Information ◽

Spatial Scales ◽

Spatial Integration ◽

Global Features ◽

Wide Range ◽

Visual Areas ◽

Higher Visual Areas

AbstractNeurons in the visual system integrate over a wide range of spatial scales. This diversity is thought to enable both local and global computations. To understand how spatial information is encoded across the mouse visual system, we use two-photon imaging to measure receptive fields in primary visual cortex (V1) and three downstream higher visual areas (HVAs): LM (lateromedial), AL (anterolateral) and PM (posteromedial). We find significantly larger receptive field sizes and less surround suppression in PM than in V1 or the other HVAs. Unlike other visual features studied in this system, specialization of spatial integration in PM cannot be explained by specific projections from V1 to the HVAs. Instead, our data suggests that distinct connectivity within PM may support the area’s unique ability to encode global features of the visual scene, whereas V1, LM and AL may be more specialized for processing local features.

Download Full-text

Laminar pattern of synaptic activity in rat primary visual cortex: comparison of in vivo and in vitro studies employing the current source density analysis

Brain Research ◽

10.1016/0006-8993(94)91421-4 ◽

1994 ◽

Vol 635 (1-2) ◽

pp. 37-48 ◽

Cited By ~ 27

Author(s):

G. Kenan-Vaknin ◽

T.J. Teyler

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Current Source ◽

Synaptic Activity ◽

Source Density ◽

Current Source Density Analysis ◽

Laminar Pattern ◽

Density Analysis

Download Full-text

1727 Roles of horizontal connection in superficial layer of the kitten primary visual cortex studied in in vivo and in vitro preparation

Neuroscience Research ◽

10.1016/0168-0102(96)89123-1 ◽

1996 ◽

Vol 25 ◽

pp. S200

Author(s):

Yumiko Yoshimura ◽

Hiromichi Sato ◽

Kazuyuki Imamura ◽

Yasuyoshi Watanabe

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Superficial Layer ◽

Horizontal Connection

Download Full-text

Neural Representation of the Luminance and Brightness of a Uniform Surface in the Macaque Primary Visual Cortex

Journal of Neurophysiology ◽

10.1152/jn.2001.86.5.2559 ◽

2001 ◽

Vol 86 (5) ◽

pp. 2559-2570 ◽

Cited By ~ 107

Author(s):

Masaharu Kinoshita ◽

Hidehiko Komatsu

Keyword(s):

Visual Cortex ◽

Receptive Field ◽

Primary Visual Cortex ◽

Neural Activity ◽

Dynamic Range ◽

Neural Representation ◽

Homogeneous Surface ◽

V1 Neurons ◽

Classical Receptive Field ◽

Multiple Unit

The perceived brightness of a surface is determined not only by the luminance of the surface (local information), but also by the luminance of its surround (global information). To better understand the neural representation of surface brightness, we investigated the effects of local and global luminance on the activity of neurons in the primary visual cortex (V1) of awake macaque monkeys. Single- and multiple-unit recordings were made from V1 while the monkeys were performing a visual fixation task. The classical receptive field of each neuron was identified as a region responding to a spot stimulus. Neural responses were assessed using homogeneous surfaces at least three times as large as the receptive field as stimuli. We first examined the sensitivity of neurons to variation in local surface luminance, while the luminance of the surround was held constant. The activity of a large majority of surface-responsive neurons (106/115) varied monotonically with changes in surface luminance; in some the dynamic range was over 3 log units. This monotonic relation between surface luminance and neural activity was more evident later in the stimulus period than early on. The effect of the global luminance on neural activity was then assessed in 81 of the surface-responsive neurons by varying the luminance of the surround while holding the luminance of the surface constant. The activity of one group of neurons (25/81) was unaffected by the luminance of the surround; these neurons appear to encode the physical luminance of a surface covering the receptive field. The responses of the other neurons were affected by the luminance of the surround. The effects of the luminances of the surface and the surround on the activities of 26 of these neurons were in the same direction (either increased or decreased), while the effects on the remaining 25 neurons were in opposite directions. The activities of the latter group of neurons seemed to parallel the perceived brightness of the surface, whereas the former seemed to encode the level of illumination. There were differences across different types of neurons with regard to the layer distribution. These findings indicate that global luminance information significantly modulates the activity of surface-responsive V1 neurons and that not only physical luminance, but also perceived brightness, of a homogeneous surface is represented in V1.

Download Full-text