scholarly journals An early phase of instructive plasticity in visual cortex before the typical onset of sensory experience

2019 ◽  
Author(s):  
Arani Roy ◽  
Shen Wang ◽  
Benyamin Meschede-Krasa ◽  
Jordan Breffle ◽  
Stephen D. Van Hooser

AbstractWhile early experience with moving stimuli is necessary for the development of direction selectivity in visual cortex of carnivores, it is unclear whether experience exerts a permissive or instructive influence. To test if the specific parameters of the experienced stimuli could instructively sculpt the emergent responses, visually naive ferrets were exposed to several hours of experience with unusual spatiotemporal patterns. In the most immature ferrets, cortical neurons developed selectivity to these patterns, indicating an instructive influence. In animals that were 1-10 days more mature, exposure to the same patterns led to a developmentally-typical increase in direction selectivity. We conclude that visual development progresses via an early phase of instructive plasticity, when the specific patterns of neural activity shape the specific parameters of the emerging response properties, followed by a late phase of permissive maturation, when sensory-driven activity merely serves to enhance the response properties already seeded in cortical circuits.

2020 ◽  
Vol 11 (1) ◽  
Author(s):  
Arani Roy ◽  
Shen Wang ◽  
Benyamin Meschede-Krasa ◽  
Jordan Breffle ◽  
Stephen D. Van Hooser

AbstractWhile early experience with moving stimuli is necessary for the development of direction selectivity in visual cortex of carnivores, it is unclear whether experience exerts a permissive or instructive influence. To test if the specific parameters of the experienced stimuli could instructively sculpt the emergent responses, visually naive ferrets were exposed to several hours of experience with unusual spatiotemporal patterns. In the most immature ferrets, cortical neurons developed selectivity to these patterns, indicating an instructive influence. In animals that were 1–10 days more mature, exposure to the same patterns led to a developmentally-typical increase in direction selectivity. We conclude that visual development progresses via an early phase of instructive plasticity, when the specific patterns of neural activity shape the specific parameters of the emerging response properties, followed by a late phase of permissive maturation, when sensory-driven activity merely serves to enhance the response properties already seeded in cortical circuits.


2005 ◽  
Vol 94 (2) ◽  
pp. 1336-1345 ◽  
Author(s):  
Bartlett D. Moore ◽  
Henry J. Alitto ◽  
W. Martin Usrey

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.


2006 ◽  
Vol 95 (4) ◽  
pp. 2705-2712 ◽  
Author(s):  
Matthew R. Peterson ◽  
Baowang Li ◽  
Ralph D. Freeman

Various properties of external scenes are integrated during the transmission of information along central visual pathways. One basic property concerns the sensitivity to direction of a moving stimulus. This direction selectivity (DS) is a fundamental response characteristic of neurons in the visual cortex. We have conducted a neurophysiological study of cells in the visual cortex to determine how DS is affected by changes in stimulus contrast. Previous work shows that a neuron integration time is increased at low contrasts, causing temporal changes of response properties. This leads to the prediction that DS should change with stimulus contrast. However, the change could be in a counterintuitive direction, i.e., DS could increase with reduced contrast. This possibility is of intrinsic interest but it is also of potential relevance to recent behavioral work in which human subjects exhibit increased DS as contrast is reduced. Our neurophysiological results are consistent with this finding, i.e., the degree of DS of cortical neurons is inversely related to stimulus contrast. Temporal phase differences of inputs to cortical cells may account for this result.


2017 ◽  
Author(s):  
Marjena Popović ◽  
Andrea K. Stacy ◽  
Mihwa Kang ◽  
Roshan Nanu ◽  
Charlotte E. Oettgen ◽  
...  

AbstractMany sensory neural circuits exhibit response normalization, which occurs when the response of a neuron to a combination of multiple stimuli is less than the sum of the responses to the individual stimuli presented alone. In the visual cortex, normalization takes the forms of cross-orientation suppression and surround suppression. At the onset of visual experience, visual circuits are partially developed and exhibit some mature features such as orientation selectivity, but it is unknown whether cross-orientation suppression or surround suppression are present at the onset of visual experience or require visual experience for their emergence. We characterized the development of these properties and their dependence on visual experience in ferrets. Visual experience was varied across three conditions: typical rearing, dark rearing, and dark rearing with daily exposure to simple sinusoidal gratings (14-16 hours total). Cross-orientation suppression and surround suppression were noted in the earliest observations, and did not vary considerably with experience. We also observed evidence of continued maturation of receptive field properties in the second month of visual experience: substantial length summation was observed only in the oldest animals (postnatal day 90); evoked firing rates were greatly increased in older animals; and direction selectivity required experience, but declined slightly in older animals. These results constrain the space of possible circuit implementations of these features.Significance StatementThe development of the brain depends on both nature – factors that are independent of the experience of an individual animal – and nurture – factors that depend on experience. While orientation selectivity, one of the major response properties of neurons in visual cortex, is already present at the onset of visual experience, it is unknown if response properties that depend on interactions among multiple stimuli develop without experience. We find that the properties of crossorientation suppression and surround suppression are present at eye opening, and do not depend on visual experience. Our results are consistent with the idea that a majority of the basic properties of sensory neurons in primary visual cortex are derived independent of the experience of an individual animal.


2021 ◽  
Author(s):  
Paolo Papale ◽  
Wietske Zuiderbaan ◽  
Rob R.M. Teeuwen ◽  
Amparo Gilhuis ◽  
Matthew W. Self ◽  
...  

Neurons in early visual cortex are not only sensitive to the image elements in their receptive field but also to the context determining whether the elements are part of an object or background. We here assessed the effect of objecthood in natural images on neuronal activity in early visual cortex, with fMRI in humans and electrophysiology in monkeys. We report that boundaries and interiors of objects elicit more activity than the background. Boundary effects occur remarkably early, implying that visual cortical neurons are tuned to features characterizing object boundaries in natural images. When a new image is presented the influence of the object interiors on neuronal activity occurs during a late phase of neuronal response and earlier when eye movements shift the image representation, implying that object representations are remapped across eye-movements. Our results reveal how object perception shapes the representation of natural images in early visual cortex.


2018 ◽  
Author(s):  
Anthony D Lien ◽  
Massimo Scanziani

AbstractDetecting the direction of an object’s motion is essential for our representation of the visual environment. Visual cortex is one of the main stages in the mammalian nervous system where motion direction may be computed de novo. Experiments and theories indicate that cortical neurons respond selectively to motion direction by combining inputs that provide information about distinct spatial locations with distinct time-delays. Despite the importance of this spatiotemporal offset for direction selectivity its origin and cellular mechanisms are not fully understood. We show that ~80+/−10 thalamic neurons responding with distinct time-courses to stimuli in distinct locations contribute to the excitation of mouse visual cortical neurons during visual stimulation. Integration of thalamic inputs with the appropriate spatiotemporal offset provides cortical neurons with the primordial bias for direction selectivity. These data show how cortical neurons selectively combine the spatiotemporal response diversity of thalamic neurons to extract fundamental features of the visual world.


2016 ◽  
Vol 115 (5) ◽  
pp. 2556-2576 ◽  
Author(s):  
Vargha Talebi ◽  
Curtis L. Baker

In the visual cortex, distinct types of neurons have been identified based on cellular morphology, response to injected current, or expression of specific markers, but neurophysiological studies have revealed visual receptive field (RF) properties that appear to be on a continuum, with only two generally recognized classes: simple and complex. Most previous studies have characterized visual responses of neurons using stereotyped stimuli such as bars, gratings, or white noise and simple system identification approaches (e.g., reverse correlation). Here we estimate visual RF models of cortical neurons using visually rich natural image stimuli and regularized regression system identification methods and characterize their spatial tuning, temporal dynamics, spatiotemporal behavior, and spiking properties. We quantitatively demonstrate the existence of three functionally distinct categories of simple cells, distinguished by their degree of orientation selectivity (isotropic or oriented) and the nature of their output nonlinearity (expansive or compressive). In addition, these three types have differing average values of several other properties. Cells with nonoriented RFs tend to have smaller RFs, shorter response durations, no direction selectivity, and high reliability. Orientation-selective neurons with an expansive output nonlinearity have Gabor-like RFs, lower spontaneous activity and responsivity, and spiking responses with higher sparseness. Oriented RFs with a compressive nonlinearity are spatially nondescript and tend to show longer response latency. Our findings indicate multiple physiologically defined types of RFs beyond the simple/complex dichotomy, suggesting that cortical neurons may have more specialized functional roles rather than lying on a multidimensional continuum.


2021 ◽  
Author(s):  
Logan Chariker ◽  
Robert Shapley ◽  
Michael Hawken ◽  
Lai-Sang Young

This paper offers a new theory for the origin of direction selectivity in the Macaque primary visual cortex, V1. Direction selectivity (DS) is essential for the perception of motion and control of pursuit eye movements. In the Macaque visual pathway, DS neurons first appear in V1, in the Simple cell population of the Magnocellular input layer 4Ca. The LGN cells that project to these cortical neurons, however, are not direction-selective. We hypothesize that DS is initiated in feedforward LGN input, in the summed responses of LGN cells afferent to a cortical cell, and it is achieved through the interplay of (a) different visual response dynamics of ON and OFF LGN cells, and (b) the wiring of ON and OFF LGN neurons to cortex. We identify specific temporal differences in the ON/OFF pathways that together with (b) produce distinct response time-courses in separated subregions; analysis and simulations confirm the efficacy of the mechanisms proposed. To constrain the theory, we present data on Simple cells in layer 4Ca in response to drifting gratings. About half of the cells were found to have high DS, and the DS was broad-band in spatial and temporal frequency (SF and TF). The proposed theory includes a complete analysis of how stimulus features such as SF and TF interact with ON/OFF dynamics and LGN-to-cortex wiring to determine the preferred direction and magnitude of DS.


2021 ◽  
Vol 44 (1) ◽  
Author(s):  
Cristopher M. Niell ◽  
Massimo Scanziani

The mouse, as a model organism to study the brain, gives us unprecedented experimental access to the mammalian cerebral cortex. By determining the cortex's cellular composition, revealing the interaction between its different components, and systematically perturbing these components, we are obtaining mechanistic insight into some of the most basic properties of cortical function. In this review, we describe recent advances in our understanding of how circuits of cortical neurons implement computations, as revealed by the study of mouse primary visual cortex. Further, we discuss how studying the mouse has broadened our understanding of the range of computations performed by visual cortex. Finally, we address how future approaches will fulfill the promise of the mouse in elucidating fundamental operations of cortex. Expected final online publication date for the Annual Review of Neuroscience, Volume 44 is July 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.


eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Yulia Bereshpolova ◽  
Xiaojuan Hei ◽  
Jose-Manuel Alonso ◽  
Harvey A Swadlow

Some cortical neurons receive highly selective thalamocortical (TC) input, but others do not. Here, we examine connectivity of single thalamic neurons (lateral geniculate nucleus, LGN) onto putative fast-spike inhibitory interneurons in layer 4 of rabbit visual cortex. We show that three ‘rules’ regulate this connectivity. These rules concern: (1) the precision of retinotopic alignment, (2) the amplitude of the postsynaptic local field potential elicited near the interneuron by spikes of the LGN neuron, and (3) the interneuron’s response latency to strong, synchronous LGN input. We found that virtually all first-order fast-spike interneurons receive input from nearly all LGN axons that synapse nearby, regardless of their visual response properties. This was not the case for neighboring regular-spiking neurons. We conclude that profuse and highly promiscuous TC inputs to layer-4 fast-spike inhibitory interneurons generate response properties that are well-suited to mediate a fast, sensitive, and broadly tuned feed-forward inhibition of visual cortical excitatory neurons.


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