scholarly journals Propagation of orientation selectivity in a spiking network model of layered primary visual cortex

2018 ◽  
Author(s):  
Benjamin Merkt ◽  
Friedrich Schüßler ◽  
Stefan Rotter
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Visual Stimulation ◽  
Orientation Selectivity ◽  
System Level ◽  
Orientation Tuning ◽  
Dimensional System ◽  
Firing Rates ◽  
Wide Range ◽  
Low Dimensional

AbstractNeurons in different layers of sensory cortex generally have different functional properties. But what determines firing rates and tuning properties of neurons in different layers? Orientation selectivity in primary visual cortex (V1) is an interesting case to study these questions. Thalamic projections essentially determine the preferred orientation of neurons that receive direct input. But how is this tuning propagated though layers, and how can selective responses emerge in layers that do not have direct access to the thalamus? Here we combine numerical simulations with mathematical analyses to address this problem. We find that a large-scale network, which just accounts for experimentally measured layer and cell-type specific connection probabilities, yields firing rates and orientation selectivities matching electrophysiological recordings in rodent V1 surprisingly well. Further analysis, however, is complicated by the fact that neuronal responses emerge in a dynamic fashion and cannot be directly inferred from static neuroanatomy, as some connections tend to have unintuitive effects due to recurrent interactions and strong feedback loops. These emergent phenomena can be understood by linearizing and coarse-graining. In fact, we were able to derive a low-dimensional linear dynamical system effectively describing stimulus-driven activity layer by layer. This low-dimensional system explains layer-specific firing rates and orientation tuning by accounting for the different gain factors of the aggregate system. Our theory can also be used to design novel optogenetic stimulation experiments, thus facilitating further exploration of the interplay between connectivity and function.Author summaryUnderstanding the precise roles of neuronal sub-populations in shaping the activity of networks is a fundamental objective of neuroscience research. In complex neuronal network structures like the neocortex, the relation between the connec-tome and the algorithm implemented in it is often not self-explaining. To this end, our work makes three important contributions. First, we show that the connectivity extracted by anatomical and physiological experiments in visual cortex suffices to explain important properties of the various sub-populations, including their selectivity to visual stimulation. Second, we introduce a novel system-level approach for the analysis of input-output relations of recurrent networks, which leads to the observed activity patterns. Third, we present a method for the design of future optogenetic experiments that can be used to devise specific stimuli resulting in a predictable change of neuronal activity. In summary, we introduce a novel frame-work to determine the relevant features of neuronal microcircuit function that can be applied to a wide range of neuronal systems.

scholarly journals Orientation Tuning, But Not Direction Selectivity, Is Invariant to Temporal Frequency in Primary Visual Cortex

2005 ◽  
Vol 94 (2) ◽  
pp. 1336-1345 ◽  
Author(s):  
Bartlett D. Moore ◽  
Henry J. Alitto ◽  
W. Martin Usrey
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Visual Stimulus ◽  
Visual Processing ◽  
Cortical Neurons ◽  
Temporal Frequency ◽  
Direction Selectivity ◽  
Orientation Tuning ◽  
Orientation Contrast ◽  
Wide Range

The activity of neurons in primary visual cortex is influenced by the orientation, contrast, and temporal frequency of a visual stimulus. This raises the question of how these stimulus properties interact to shape neuronal responses. While past studies have shown that the bandwidth of orientation tuning is invariant to stimulus contrast, the influence of temporal frequency on orientation-tuning bandwidth is unknown. Here, we investigate the influence of temporal frequency on orientation tuning and direction selectivity in area 17 of ferret visual cortex. For both simple cells and complex cells, measures of orientation-tuning bandwidth (half-width at half-maximum response) are ∼20–25° across a wide range of temporal frequencies. Thus cortical neurons display temporal-frequency invariant orientation tuning. In contrast, direction selectivity is typically reduced, and occasionally reverses, at nonpreferred temporal frequencies. These results show that the mechanisms contributing to the generation of orientation tuning and direction selectivity are differentially affected by the temporal frequency of a visual stimulus and support the notion that stability of orientation tuning is an important aspect of visual processing.

scholarly journals Orientation Tuning of Input Conductance, Excitation, and Inhibition in Cat Primary Visual Cortex

2000 ◽  
Vol 84 (2) ◽  
pp. 909-926 ◽  
Author(s):  
Jeffrey S. Anderson ◽  
Matteo Carandini ◽  
David Ferster
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Visual Stimulation ◽  
Gain Control ◽  
Orientation Tuning ◽  
Visual Responses ◽  
Stimulus Contrast ◽  
Simple Cells ◽  
Conductance Changes ◽  
Input Conductance

The input conductance of cells in the cat primary visual cortex (V1) has been shown recently to grow substantially during visual stimulation. Because increasing conductance can have a divisive effect on the synaptic input, theoretical proposals have ascribed to it specific functions. According to the veto model, conductance increases would serve to sharpen orientation tuning by increasing most at off-optimal orientations. According to the normalization model, conductance increases would control the cell's gain, by being independent of stimulus orientation and by growing with stimulus contrast. We set out to test these proposals and to determine the visual properties and possible synaptic origin of the conductance increases. We recorded the membrane potential of cat V1 cells while injecting steady currents and presenting drifting grating patterns of varying contrast and orientation. Input conductance grew with stimulus contrast by 20–300%, generally more in simple cells (40–300%) than in complex cells (20–120%), and in simple cells was strongly modulated in time. Conductance was invariably maximal for stimuli of the preferred orientation. Thus conductance changes contribute to a gain control mechanism, but the strength of this gain control does not depend uniquely on contrast. By assuming that the conductance changes are entirely synaptic, we further derived the excitatory and inhibitory synaptic conductances underlying the visual responses. In simple cells, these conductances were often arranged in push-pull: excitation increased when inhibition decreased and vice versa. Excitation and inhibition had similar preferred orientations and did not appear to differ in tuning width, suggesting that the intracortical synaptic inputs to simple cells of cat V1 originate from cells with similar orientation tuning. This finding is at odds with models where orientation tuning in simple cells is achieved by inhibition at off-optimal orientations or sharpened by inhibition that is more broadly tuned than excitation.

scholarly journals Orientation selectivity in the visual cortex of the nine-banded armadillo

2017 ◽  
Vol 117 (3) ◽  
pp. 1395-1406 ◽  
Author(s):  
Benjamin Scholl ◽  
Johnathan Rylee ◽  
Jeffrey J. Luci ◽  
Nicholas J. Priebe ◽  
Jeffrey Padberg
Keyword(s):  
Visual Cortex ◽  
Functional Properties ◽  
Primary Visual Cortex ◽  
Functional Organization ◽  
Orientation Selectivity ◽  
Small Subset ◽  
Motion Direction ◽  
V1 Neurons ◽  
Wide Range ◽  
Degree Of Orientation

Orientation selectivity in primary visual cortex (V1) has been proposed to reflect a canonical computation performed by the neocortical circuitry. Although orientation selectivity has been reported in all mammals examined to date, the degree of selectivity and the functional organization of selectivity vary across mammalian clades. The differences in degree of orientation selectivity are large, from reports in marsupials that only a small subset of neurons are selective to studies in carnivores, in which it is rare to find a neuron lacking selectivity. Furthermore, the functional organization in cortex varies in that the primate and carnivore V1 is characterized by an organization in which nearby neurons share orientation preference while other mammals such as rodents and lagomorphs either lack or have only extremely weak clustering. To gain insight into the evolutionary emergence of orientation selectivity, we examined the nine-banded armadillo, a species within the early placental clade Xenarthra. Here we use a combination of neuroimaging, histological, and electrophysiological methods to identify the retinofugal pathways, locate V1, and for the first time examine the functional properties of V1 neurons in the armadillo ( Dasypus novemcinctus) V1. Individual neurons were strongly sensitive to the orientation and often the direction of drifting gratings. We uncovered a wide range of orientation preferences but found a bias for horizontal gratings. The presence of strong orientation selectivity in armadillos suggests that the circuitry responsible for this computation is common to all placental mammals.NEW & NOTEWORTHY The current study shows that armadillo primary visual cortex (V1) neurons share the signature properties of V1 neurons of primates, carnivorans, and rodents. Furthermore, these neurons exhibit a degree of selectivity for stimulus orientation and motion direction similar to that found in primate V1. Our findings in armadillo visual cortex suggest that the functional properties of V1 neurons emerged early in the mammalian lineage, near the time of the divergence of marsupials.

scholarly journals Stimulus Vignetting and Orientation Selectivity in Human Visual Cortex

2018 ◽  
Author(s):  
Zvi N. Roth ◽  
David J. Heeger ◽  
Elisha P. Merriam
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Large Body ◽  
Orientation Selectivity ◽  
Orientation Tuning ◽  
Neural Responses ◽  
Macroscopic Scale ◽  
Sensory Features ◽  
Neural Selectivity ◽  
The Impact

AbstractNeural selectivity to orientation is one of the simplest and most thoroughly-studied cortical sensory features. Here, we show that a large body of research that purported to measure orientation tuning may have in fact been inadvertently measuring sensitivity to second-order changes in luminance, a phenomenon we term ‘vignetting’. Using a computational model of neural responses in primary visual cortex (V1), we demonstrate the impact of vignetting on simulated V1 responses. We then used the model to generate a set of predictions, which we confirmed with functional MRI experiments in human observers. Our results demonstrate that stimulus vignetting can wholly determine the orientation selectivity of responses in visual cortex measured at a macroscopic scale, and suggest a reinterpretation of a well-established literature on orientation processing in visual cortex.

scholarly journals Stimulus vignetting and orientation selectivity in human visual cortex

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Zvi N Roth ◽  
David J Heeger ◽  
Elisha P Merriam
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Large Body ◽  
Orientation Selectivity ◽  
Orientation Tuning ◽  
Neural Responses ◽  
Macroscopic Scale ◽  
Sensory Features ◽  
Neural Selectivity ◽  
The Impact

Neural selectivity to orientation is one of the simplest and most thoroughly-studied cortical sensory features. Here, we show that a large body of research that purported to measure orientation tuning may have in fact been inadvertently measuring sensitivity to second-order changes in luminance, a phenomenon we term ‘vignetting'. Using a computational model of neural responses in primary visual cortex (V1), we demonstrate the impact of vignetting on simulated V1 responses. We then used the model to generate a set of predictions, which we confirmed with functional MRI experiments in human observers. Our results demonstrate that stimulus vignetting can wholly determine the orientation selectivity of responses in visual cortex measured at a macroscopic scale, and suggest a reinterpretation of a well-established literature on orientation processing in visual cortex.

scholarly journals Mechanisms underlying contrast-dependent orientation selectivity in mouse V1

2018 ◽  
Vol 115 (45) ◽  
pp. 11619-11624 ◽  
Author(s):  
Wei P. Dai ◽  
Douglas Zhou ◽  
David W. McLaughlin ◽  
David Cai
Keyword(s):  
Large Scale ◽  
Feedback Inhibition ◽  
Orientation Selectivity ◽  
Inhibitory Neurons ◽  
Orientation Tuning ◽  
Response Properties ◽  
Firing Rates ◽  
Excitatory Neurons ◽  
Cortical Excitation ◽  
Contrast Invariance

Recent experiments have shown that mouse primary visual cortex (V1) is very different from that of cat or monkey, including response properties—one of which is that contrast invariance in the orientation selectivity (OS) of the neurons’ firing rates is replaced in mouse with contrast-dependent sharpening (broadening) of OS in excitatory (inhibitory) neurons. These differences indicate a different circuit design for mouse V1 than that of cat or monkey. Here we develop a large-scale computational model of an effective input layer of mouse V1. Constrained by experiment data, the model successfully reproduces experimentally observed response properties—for example, distributions of firing rates, orientation tuning widths, and response modulations of simple and complex neurons, including the contrast dependence of orientation tuning curves. Analysis of the model shows that strong feedback inhibition and strong orientation-preferential cortical excitation to the excitatory population are the predominant mechanisms underlying the contrast-sharpening of OS in excitatory neurons, while the contrast-broadening of OS in inhibitory neurons results from a strong but nonpreferential cortical excitation to these inhibitory neurons, with the resulting contrast-broadened inhibition producing a secondary enhancement on the contrast-sharpened OS of excitatory neurons. Finally, based on these mechanisms, we show that adjusting the detailed balances between the predominant mechanisms can lead to contrast invariance—providing insights for future studies on contrast dependence (invariance).

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