scholarly journals Development of cross-orientation suppression and size tuning and the role of experience

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.

1985 ◽  
Vol 53 (2) ◽  
pp. 572-589 ◽  
Author(s):  
G. D. Mower ◽  
W. G. Christen

Cats were reared in total darkness from birth until 4-5 mo of age (DR cats, n = 7) or with very brief visual experience (1 or 2 days) during an otherwise similar period of dark rearing [DR(1) cats, n = 3; DR(2) cats, n = 7]. Single-cell recordings were made in area 17 of visual cortex at the end of this rearing period and/or after a subsequent prolonged period of monocular deprivation. Control observations were made in normal cats (n = 3), cats reared with monocular deprivation from birth (n = 4), and cats monocularly deprived after being reared normally until 4 mo of age (n = 2). After rearing cats in total darkness, the majority of visual cortical cells were binocularly driven and the overall distribution of ocular dominance was not different from that of normal cats. Orientation-selective cells were very rare in dark-reared cats. Monocular deprivation imposed after dark rearing resulted in selective development of connections from the open eye. Most cells were responsive only to the open eye and the majority of these were orientation selective. These results were similar to, though less severe than, those found in cats reared with monocular deprivation from birth. Monocular deprivation imposed after 4 mo of normal rearing did not produce selective development of connections from the open eye in terms of either ocular dominance or orientation selectivity. In DR(1) cats visual cortical physiology was degraded in comparison to dark-reared cats after the rearing period. Most cells were binocularly driven but there was a higher frequency of unresponsive cells and a reduced frequency of orientation-selective cells. Subsequent monocular deprivation resulted in a further decrease in the number of binocularly driven cells and an increase in unresponsive cells. However, it did not produce a bias in favor of the open eye in terms of either ocular dominance or orientation selectivity. In DR(2) cats there was a high incidence of unresponsive cells and a marked loss of binocularly driven cells after the rearing period. Subsequent monocular deprivation failed to produce any significant changes.(ABSTRACT TRUNCATED AT 400 WORDS)


1994 ◽  
Vol 34 (6) ◽  
pp. 709-720 ◽  
Author(s):  
Michela Fagiolini ◽  
Tommaso Pizzorusso ◽  
Nicoletta Berardi ◽  
Luciano Domenici ◽  
Lamberto Maffei

2002 ◽  
Vol 88 (4) ◽  
pp. 1933-1940 ◽  
Author(s):  
Chris J. Beaver ◽  
Quentin S. Fischer ◽  
Qinghua Ji ◽  
Nigel W. Daw

We have previously shown that the protein kinase A (PKA) inhibitor, 8-chloroadenosine-3′,5′–monophosphorothioate (Rp-8-Cl-cAMPS), abolishes ocular dominance plasticity in the cat visual cortex. Here we investigate the effect of this inhibitor on orientation selectivity. The inhibitor reduces orientation selectivity in monocularly deprived animals but not in normal animals. In other words, PKA inhibitors by themselves do not affect orientation selectivity, nor does monocular deprivation by itself, but monocular deprivation in combination with a PKA inhibitor does affect orientation selectivity. This result is found for the receptive fields in both deprived and nondeprived eyes. Although there is a tendency for the orientation selectivity in the nondeprived eye to be higher than the orientation selectivity in the deprived eye, the orientation selectivity in both eyes is considerably less than normal. The result is striking in animals at 4 wk of age. The effect of the monocular deprivation on orientation selectivity is reduced at 6 wk of age and absent at 9 wk of age, while the effect on ocular dominance shifts is less changed in agreement with previous results showing that the critical period for orientation/direction selectivity ends earlier than the critical period for ocular dominance. We conclude that closure of one eye in combination with inhibition of PKA reduces orientation selectivity during the period that orientation selectivity is still mutable and that the reduction in orientation selectivity is transferred to the nondeprived eye.


2016 ◽  
Author(s):  
Inbal Ayzenshtat ◽  
Jesse Jackson ◽  
Rafael Yuste

AbstractThe response properties of neurons to sensory stimuli have been used to identify their receptive fields and functionally map sensory systems. In primary visual cortex, most neurons are selective to a particular orientation and spatial frequency of the visual stimulus. Using two-photon calcium imaging of neuronal populations from the primary visual cortex of mice, we have characterized the response properties of neurons to various orientations and spatial frequencies. Surprisingly, we found that the orientation selectivity of neurons actually depends on the spatial frequency of the stimulus. This dependence can be easily explained if one assumed spatially asymmetric Gabor-type receptive fields. We propose that receptive fields of neurons in layer 2/3 of visual cortex are indeed spatially asymmetric, and that this asymmetry could be used effectively by the visual system to encode natural scenes.Significance StatementIn this manuscript we demonstrate that the orientation selectivity of neurons in primary visual cortex of mouse is highly dependent on the stimulus SF. This dependence is realized quantitatively in a decrease in the selectivity strength of cells in non-optimum SF, and more importantly, it is also evident qualitatively in a shift in the preferred orientation of cells in non-optimum SF. We show that a receptive-field model of a 2D asymmetric Gabor, rather than a symmetric one, can explain this surprising observation. Therefore, we propose that the receptive fields of neurons in layer 2/3 of mouse visual cortex are spatially asymmetric and this asymmetry could be used effectively by the visual system to encode natural scenes.Highlights–Orientation selectivity is dependent on spatial frequency.–Asymmetric Gabor model can explain this dependence.


2006 ◽  
Vol 9 (5) ◽  
pp. 676-681 ◽  
Author(s):  
Ye Li ◽  
David Fitzpatrick ◽  
Leonard E White

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.


2003 ◽  
Vol 89 (2) ◽  
pp. 1003-1015 ◽  
Author(s):  
W. Martin Usrey ◽  
Michael P. Sceniak ◽  
Barbara Chapman

The ferret has become a model animal for studies exploring the development of the visual system. However, little is known about the receptive-field structure and response properties of neurons in the adult visual cortex of the ferret. We performed single-unit recordings from neurons in layer 4 of adult ferret primary visual cortex to determine the receptive-field structure and visual-response properties of individual neurons. In particular, we asked what is the spatiotemporal structure of receptive fields of layer 4 neurons and what is the orientation selectivity of layer 4 neurons? Receptive fields of layer 4 neurons were mapped using a white-noise stimulus; orientation selectivity was determined using drifting, sine-wave gratings. Our results show that most neurons (84%) within layer 4 are simple cells with elongated, spatially segregated,on and off subregions. These neurons are also selective for stimulus orientation; peaks in orientation-tuning curves have, on average, a half-width at half-maximum response of 21.5 ± 1.2° (mean ± SD). The remaining neurons in layer 4 (16%) lack orientation selectivity and have center/surround receptive fields. Although the organization of geniculate inputs to layer 4 differs substantially between ferret and cat, our results demonstrate that, like in the cat, most neurons in ferret layer 4 are orientation-selective simple cells.


1986 ◽  
Vol 56 (4) ◽  
pp. 1074-1087 ◽  
Author(s):  
H. D. Schwark ◽  
J. G. Malpeli ◽  
T. G. Weyand ◽  
C. Lee

Response properties of cells in the infragranular layers of cortical area 17 of the cat were examined in the absence of input from supragranular layers. Supragranular activity was silenced either reversibly by cooling the surface of cortex or permanently by making a cryogenic lesion of the supragranular layers. Visually driven responses of cells throughout the cortical column were recorded with a linear array of electrodes. Most infragranular layer cells continued to be visually responsive in the absence of supragranular layer input. These cells were similar to normal infragranular layer cells on measures of visual responsiveness, orientation selectivity, and direction selectivity. Special complex, but not standard complex, cells were absent in layer 5 when supragranular layers were destroyed. We found no evidence for a selective effect of removal of supragranular activity on the response properties of cells in layer 6. We propose that the intracolumnar projection from the supragranular layers drives the special complex cells of layer 5, but is not necessary for the visual driving of most other infragranular layer cells. This projection does not impose selectivity for stimulus orientation or direction on the remaining active cells of the infragranular layers.


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