Prior expectations evoke stimulus-specific activity in the deep layers of the primary visual cortex

AbstractThe way we perceive the world is strongly influenced by our expectations. In line with this, much recent research has revealed that prior expectations strongly modulate sensory processing. However, the neural circuitry through which the brain integrates external sensory inputs with internal expectation signals remains unknown. In order to understand the computational architecture of the cortex, we need to investigate the way these signals flow through the cortical layers. This is crucial because the different cortical layers have distinct intra- and interregional connectivity patterns, and therefore determining which layers are involved in a cortical computation can inform us on the sources and targets of these signals. Here, we used ultra-high field (7T) functional magnetic resonance imaging (fMRI) to reveal that prior expectations evoke stimulus templates selectively in the deep layers of the primary visual cortex. These results shed light on the neural circuit underlying perceptual inference.

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Perceived and mentally rotated contents are differentially represented in cortical depth of V1

Communications Biology ◽

10.1038/s42003-021-02582-4 ◽

2021 ◽

Vol 4 (1) ◽

Author(s):

Polina Iamshchinina ◽

Daniel Kaiser ◽

Renat Yakupov ◽

Daniel Haenelt ◽

Alessandro Sciarra ◽

...

Keyword(s):

Visual Cortex ◽

High Resolution ◽

Mental Rotation ◽

Primary Visual Cortex ◽

External Input ◽

General Strategy ◽

Cortical Layers ◽

Early Visual Cortex ◽

Feedback Connections ◽

The Brain

AbstractPrimary visual cortex (V1) in humans is known to represent both veridically perceived external input and internally-generated contents underlying imagery and mental rotation. However, it is unknown how the brain keeps these contents separate thus avoiding a mixture of the perceived and the imagined which could lead to potentially detrimental consequences. Inspired by neuroanatomical studies showing that feedforward and feedback connections in V1 terminate in different cortical layers, we hypothesized that this anatomical compartmentalization underlies functional segregation of external and internally-generated visual contents, respectively. We used high-resolution layer-specific fMRI to test this hypothesis in a mental rotation task. We found that rotated contents were predominant at outer cortical depth bins (i.e. superficial and deep). At the same time perceived contents were represented stronger at the middle cortical bin. These results identify how through cortical depth compartmentalization V1 functionally segregates rather than confuses external from internally-generated visual contents. These results indicate that feedforward and feedback manifest in distinct subdivisions of the early visual cortex, thereby reflecting a general strategy for implementing multiple cognitive functions within a single brain region.

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Perceived and mentally rotated contents are differentially represented in cortical depth of V1

10.1101/2021.04.27.440989 ◽

2021 ◽

Author(s):

Polina Iamshchinina ◽

Daniel Kaiser ◽

Renat Yakupov ◽

Daniel Haenelt ◽

Alessandro Sciarra ◽

...

Keyword(s):

Visual Cortex ◽

High Resolution ◽

Mental Rotation ◽

Primary Visual Cortex ◽

External Input ◽

General Strategy ◽

Cortical Layers ◽

Early Visual Cortex ◽

Feedback Connections ◽

The Brain

AbstractPrimary visual cortex (V1) in humans is known to represent both veridically perceived external input and internally-generated contents underlying imagery and mental rotation. However, it is unknown how the brain keeps these contents separate thus avoiding a mixture of the perceived and the imagined which could lead to potentially detrimental consequences. Inspired by neuroanatomical studies showing that feedforward and feedback connections in V1 terminate in different cortical layers, we hypothesized that this anatomical compartmentalization underlies functional segregation of external and internally-generated visual contents, respectively. We used high-resolution layer-specific fMRI to test this hypothesis in a mental rotation task. We found that rotated contents were predominant at outer cortical depth bins (i.e. superficial and deep). At the same time perceived contents were represented stronger at the middle cortical bin. These results identify how through cortical depth compartmentalization V1 functionally segregates rather than confuses external from internally-generated visual contents. These results indicate that feedforward and feedback manifest in distinct subdivisions of the early visual cortex, thereby reflecting a general strategy for implementing multiple cognitive functions within a single brain region.

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Distinct Laminar Processing of Local and Global Context in Primate Primary Visual Cortex

10.1101/171793 ◽

2017 ◽

Cited By ~ 2

Author(s):

Maryam Bijanzadeh ◽

Lauri Nurminen ◽

Sam Merlin ◽

Alessandra Angelucci

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Visual Space ◽

Spatial Context ◽

Surround Suppression ◽

Cortical Layers ◽

Global Context ◽

Global Signal ◽

Deep Layers ◽

Contextual Stimuli

Visual perception is profoundly affected by spatial context. In visual cortex, neuronal responses to stimuli inside their receptive field (RF) are suppressed by contextual stimuli in the RF surround (surround suppression). How do neuronal RFs integrate information across visual space, and what role do different cortical layers play in the processing of spatial context? By recording simultaneously across all layers of macaque primary visual cortex, while presenting visual stimuli at increasing distances from the recorded cells RF, we find that near vs. far stimuli activate distinct layers. Stimuli in the near-surround evoke the earliest subthreshold responses in superficial and deep layers, and cause the earliest surround suppression of spiking responses in superficial layers. Instead, far-surround stimuli evoke the earliest subthreshold responses in feedback-recipient layers, i.e. 1 and the lower half of the deep layers, and suppress visually-evoked spiking responses almost simultaneously in all layers, except 4C, where suppression emerges latest. Our results reveal unique contributions of the cortical layers to the processing of local and global spatial context, and suggest distinct underlying circuits for local and global signal integration.

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Head Movements Control the Activity of Primary Visual Cortex in a Luminance Dependent Manner

10.1101/2020.01.20.913160 ◽

2020 ◽

Cited By ~ 1

Author(s):

Guy Bouvier ◽

Yuta Senzai ◽

Massimo Scanziani

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Head Movements ◽

Inhibitory Neurons ◽

Dependent Manner ◽

Ambient Light ◽

Cortical Circuits ◽

Cortical Layers ◽

Visual Cortical ◽

The Brain

AbstractThe vestibular system broadcasts head-movement related signals to sensory areas throughout the brain, including visual cortex. These signals are crucial for the brain’s ability to assess whether motion of the visual scene results from the animal’s head-movements. How head-movements impact visual cortical circuits remains, however, poorly understood. Here, we discover that ambient luminance profoundly transforms how mouse primary visual cortex (V1) processes head-movements. While in darkness, head movements result in an overall suppression of neuronal activity, in ambient light the same head movements trigger excitation across all cortical layers. This light-dependent switch in how V1 processes head-movements is controlled by somatostatin expressing (SOM) inhibitory neurons, which are excited by head movements in dark but not in light. This study thus reveals a light-dependent switch in the response of V1 to head-movements and identifies a circuit in which SOM cells are key integrators of vestibular and luminance signals.

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Homeostatic plasticity mechanisms in mouse V1

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2016.0504 ◽

2017 ◽

Vol 372 (1715) ◽

pp. 20160504 ◽

Cited By ~ 10

Author(s):

Megumi Kaneko ◽

Michael P. Stryker

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Neuronal Activity ◽

Dynamic Range ◽

Ocular Dominance ◽

Homeostatic Plasticity ◽

Ocular Dominance Plasticity ◽

The Brain

Mechanisms thought of as homeostatic must exist to maintain neuronal activity in the brain within the dynamic range in which neurons can signal. Several distinct mechanisms have been demonstrated experimentally. Three mechanisms that act to restore levels of activity in the primary visual cortex of mice after occlusion and restoration of vision in one eye, which give rise to the phenomenon of ocular dominance plasticity, are discussed. The existence of different mechanisms raises the issue of how these mechanisms operate together to converge on the same set points of activity. This article is part of the themed issue ‘Integrating Hebbian and homeostatic plasticity’.

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Blindsight and Unconscious Vision: What They Teach Us about the Human Visual System

The Neuroscientist ◽

10.1177/1073858416673817 ◽

2016 ◽

Vol 23 (5) ◽

pp. 529-541 ◽

Cited By ~ 18

Author(s):

Sara Ajina ◽

Holly Bridge

Keyword(s):

Visual Cortex ◽

Visual System ◽

Primary Visual Cortex ◽

Neural Activity ◽

Human Visual System ◽

Visual Information ◽

Visual Loss ◽

Physiological Conditions ◽

The World ◽

The Brain

Damage to the primary visual cortex removes the major input from the eyes to the brain, causing significant visual loss as patients are unable to perceive the side of the world contralateral to the damage. Some patients, however, retain the ability to detect visual information within this blind region; this is known as blindsight. By studying the visual pathways that underlie this residual vision in patients, we can uncover additional aspects of the human visual system that likely contribute to normal visual function but cannot be revealed under physiological conditions. In this review, we discuss the residual abilities and neural activity that have been described in blindsight and the implications of these findings for understanding the intact system.

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Selective Activation of the Deep Layers of the Human Primary Visual Cortex by Top-Down Feedback

Current Biology ◽

10.1016/j.cub.2015.12.038 ◽

2016 ◽

Vol 26 (3) ◽

pp. 371-376 ◽

Cited By ~ 178

Author(s):

Peter Kok ◽

Lauren J. Bains ◽

Tim van Mourik ◽

David G. Norris ◽

Floris P. de Lange

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Top Down ◽

Selective Activation ◽

Deep Layers

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Do Rotation Coordinates Provide the Substrate for a Mental Protractor?

Perception ◽

10.1068/p5338 ◽

2005 ◽

Vol 34 (11) ◽

pp. 1339-1352 ◽

Cited By ~ 1

Author(s):

Ernest Greene ◽

William Frawley

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Angular Position ◽

Spatial Position ◽

Angular Measure ◽

Relative Angle ◽

Brain Maps ◽

The Subject ◽

The Brain

In previous studies, we have found that the accuracy in judging collinearity of lines or dots varies considerably from one subject to another as a function of the relative angle of the stimulus elements. A model of errors generally shows large excursions across several subranges of angular position. These do not appear to be motor errors, at least not ones that are well separated from perceptual mechanisms. The errors are most likely generated at primary visual cortex, or beyond. We examined and modeled accuracy in judging collinearity of dot pairs, varying the angular position of the dots through 360°, the distance between the dots (stimulus span), and the distance at which the subject was required to respond (response span). Subjects manifested idiosyncratic profiles of error across angular positions, as reported previously. But across the tested range of spans, from 4 to 8 deg, the errors tended to be the same, irrespective of stimulus or response span. This suggests that the judgments are based on a radial (angular) measure of spatial position. We discuss these results in the context of proposals that the brain maps spatial position using rotation coordinates. These new data are consistent with the hypothesis that subjects use the z-axis coordinates as a mental protractor for judging angular position and collinearity.

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Running reduces firing but improves coding in rodent higher-order visual cortex

10.1101/214007 ◽

2017 ◽

Cited By ~ 7

Author(s):

Amelia J. Christensen ◽

Jonathan W. Pillow

Keyword(s):

Visual Cortex ◽

Primary Visual Cortex ◽

Single Neuron ◽

Higher Order ◽

Visual Responses ◽

Cortical Layers ◽

Response Properties ◽

Stimulus Response ◽

Allen Brain ◽

Visual Areas

Running profoundly alters stimulus-response properties in mouse primary visual cortex (V1), but its effects in higher-order visual cortex remain unknown. Here we systematically investigated how locomotion modulates visual responses across six visual areas and three cortical layers using a massive dataset from the Allen Brain Institute. Although running has been shown to increase firing in V1, we found that it suppressed firing in higher-order visual areas. Despite this reduction in gain, visual responses during running could be decoded more accurately than visual responses during stationary periods. We show that this effect was not attributable to changes in noise correlations, and propose that it instead arises from increased reliability of single neuron responses during running.

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