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Supranormal orientation selectivity of visual neurons in orientation-restricted animals.

Sasaki KS, Kimura R, Ninomiya T, Tabuchi Y, Tanaka H, Fukui M, Asada YC, Arai T, Inagaki M, Nakazono T, Baba M, Kato D, Nishimoto S, Sanada TM, Tani T, Imamura K, Tanaka S, Ohzawa I - Sci Rep (2015)

Bottom Line: Our results demonstrate that restricted sensory experiences can sculpt the supranormal functions of single neurons tailored for a particular environment.The above findings, in addition to the minimal population response to orientations close to the experienced one, agree with the predictions of a sparse coding hypothesis in which information is represented efficiently by a small number of activated neurons.This suggests that early brain areas adopt an efficient strategy for coding information even when animals are raised in a severely limited visual environment where sensory inputs have an unnatural statistical structure.

View Article: PubMed Central - PubMed

Affiliation: Graduate School of Frontier Biosciences, Osaka University, Suita, Osaka 565-0871, Japan.

ABSTRACT
Altered sensory experience in early life often leads to remarkable adaptations so that humans and animals can make the best use of the available information in a particular environment. By restricting visual input to a limited range of orientations in young animals, this investigation shows that stimulus selectivity, e.g., the sharpness of tuning of single neurons in the primary visual cortex, is modified to match a particular environment. Specifically, neurons tuned to an experienced orientation in orientation-restricted animals show sharper orientation tuning than neurons in normal animals, whereas the opposite was true for neurons tuned to non-experienced orientations. This sharpened tuning appears to be due to elongated receptive fields. Our results demonstrate that restricted sensory experiences can sculpt the supranormal functions of single neurons tailored for a particular environment. The above findings, in addition to the minimal population response to orientations close to the experienced one, agree with the predictions of a sparse coding hypothesis in which information is represented efficiently by a small number of activated neurons. This suggests that early brain areas adopt an efficient strategy for coding information even when animals are raised in a severely limited visual environment where sensory inputs have an unnatural statistical structure.

No MeSH data available.


Orientation restriction with v-goggles.(a) Typical experiment schedule. (b) Simulated defocus by cylindrical lenses. Left, Original natural image. Small image patches are extracted to show local orientation structures (magnified ×1.75). Right, Defocused image (+67 diopter). Note the disappearance of horizontal and oblique features. The photograph was taken by K. S. Sasaki. (c) Top left, Cortical image of area 17/18. Top right, Orientation map by intrinsic optical imaging at 36 days after birth. Colour and brightness indicate the preferred orientation and signal magnitude, respectively. The average of responses at 0.15 and 0.5 cpd is shown. The white border delineates the extent of area 17 where 0.5 cpd gratings elicited higher responses than 0.15 cpd gratings. Bottom, Distribution of preferred orientations. The black bars show the distribution for strongly orientation-selective pixels (circular variance [CV] < 0.8). The dashed horizontal line indicates expected values for a uniform distribution.
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f1: Orientation restriction with v-goggles.(a) Typical experiment schedule. (b) Simulated defocus by cylindrical lenses. Left, Original natural image. Small image patches are extracted to show local orientation structures (magnified ×1.75). Right, Defocused image (+67 diopter). Note the disappearance of horizontal and oblique features. The photograph was taken by K. S. Sasaki. (c) Top left, Cortical image of area 17/18. Top right, Orientation map by intrinsic optical imaging at 36 days after birth. Colour and brightness indicate the preferred orientation and signal magnitude, respectively. The average of responses at 0.15 and 0.5 cpd is shown. The white border delineates the extent of area 17 where 0.5 cpd gratings elicited higher responses than 0.15 cpd gratings. Bottom, Distribution of preferred orientations. The black bars show the distribution for strongly orientation-selective pixels (circular variance [CV] < 0.8). The dashed horizontal line indicates expected values for a uniform distribution.

Mentions: Orientation restriction provides an opportunity to evaluate quantitatively how structured visual experiences influence the functional development of single neurons in a manipulated environment. To guarantee that the animals always experienced a particular orientation, we fabricated goggles with cylindrical lenses (+67 diopter) that allow optical patterns to be transmitted in a severely restricted orientation range (90° ± 12° at 0.5 cycles/degree [cpd], 90° ± 38° at 0.15 cpd)67. These goggles (v-goggles) were chronically mounted on a kitten’s head securely at approximately 3 weeks after birth so that it experienced the vertical orientation exclusively throughout its life (Fig. 1).


Supranormal orientation selectivity of visual neurons in orientation-restricted animals.

Sasaki KS, Kimura R, Ninomiya T, Tabuchi Y, Tanaka H, Fukui M, Asada YC, Arai T, Inagaki M, Nakazono T, Baba M, Kato D, Nishimoto S, Sanada TM, Tani T, Imamura K, Tanaka S, Ohzawa I - Sci Rep (2015)

Orientation restriction with v-goggles.(a) Typical experiment schedule. (b) Simulated defocus by cylindrical lenses. Left, Original natural image. Small image patches are extracted to show local orientation structures (magnified ×1.75). Right, Defocused image (+67 diopter). Note the disappearance of horizontal and oblique features. The photograph was taken by K. S. Sasaki. (c) Top left, Cortical image of area 17/18. Top right, Orientation map by intrinsic optical imaging at 36 days after birth. Colour and brightness indicate the preferred orientation and signal magnitude, respectively. The average of responses at 0.15 and 0.5 cpd is shown. The white border delineates the extent of area 17 where 0.5 cpd gratings elicited higher responses than 0.15 cpd gratings. Bottom, Distribution of preferred orientations. The black bars show the distribution for strongly orientation-selective pixels (circular variance [CV] < 0.8). The dashed horizontal line indicates expected values for a uniform distribution.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4644951&req=5

f1: Orientation restriction with v-goggles.(a) Typical experiment schedule. (b) Simulated defocus by cylindrical lenses. Left, Original natural image. Small image patches are extracted to show local orientation structures (magnified ×1.75). Right, Defocused image (+67 diopter). Note the disappearance of horizontal and oblique features. The photograph was taken by K. S. Sasaki. (c) Top left, Cortical image of area 17/18. Top right, Orientation map by intrinsic optical imaging at 36 days after birth. Colour and brightness indicate the preferred orientation and signal magnitude, respectively. The average of responses at 0.15 and 0.5 cpd is shown. The white border delineates the extent of area 17 where 0.5 cpd gratings elicited higher responses than 0.15 cpd gratings. Bottom, Distribution of preferred orientations. The black bars show the distribution for strongly orientation-selective pixels (circular variance [CV] < 0.8). The dashed horizontal line indicates expected values for a uniform distribution.
Mentions: Orientation restriction provides an opportunity to evaluate quantitatively how structured visual experiences influence the functional development of single neurons in a manipulated environment. To guarantee that the animals always experienced a particular orientation, we fabricated goggles with cylindrical lenses (+67 diopter) that allow optical patterns to be transmitted in a severely restricted orientation range (90° ± 12° at 0.5 cycles/degree [cpd], 90° ± 38° at 0.15 cpd)67. These goggles (v-goggles) were chronically mounted on a kitten’s head securely at approximately 3 weeks after birth so that it experienced the vertical orientation exclusively throughout its life (Fig. 1).

Bottom Line: Our results demonstrate that restricted sensory experiences can sculpt the supranormal functions of single neurons tailored for a particular environment.The above findings, in addition to the minimal population response to orientations close to the experienced one, agree with the predictions of a sparse coding hypothesis in which information is represented efficiently by a small number of activated neurons.This suggests that early brain areas adopt an efficient strategy for coding information even when animals are raised in a severely limited visual environment where sensory inputs have an unnatural statistical structure.

View Article: PubMed Central - PubMed

Affiliation: Graduate School of Frontier Biosciences, Osaka University, Suita, Osaka 565-0871, Japan.

ABSTRACT
Altered sensory experience in early life often leads to remarkable adaptations so that humans and animals can make the best use of the available information in a particular environment. By restricting visual input to a limited range of orientations in young animals, this investigation shows that stimulus selectivity, e.g., the sharpness of tuning of single neurons in the primary visual cortex, is modified to match a particular environment. Specifically, neurons tuned to an experienced orientation in orientation-restricted animals show sharper orientation tuning than neurons in normal animals, whereas the opposite was true for neurons tuned to non-experienced orientations. This sharpened tuning appears to be due to elongated receptive fields. Our results demonstrate that restricted sensory experiences can sculpt the supranormal functions of single neurons tailored for a particular environment. The above findings, in addition to the minimal population response to orientations close to the experienced one, agree with the predictions of a sparse coding hypothesis in which information is represented efficiently by a small number of activated neurons. This suggests that early brain areas adopt an efficient strategy for coding information even when animals are raised in a severely limited visual environment where sensory inputs have an unnatural statistical structure.

No MeSH data available.