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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 and spatial frequency tuning of single neurons.The orientation and spatial frequency tuning parameters of individual neurons were obtained by fitting a Gaussian function to the response surfaces of each cell (Fig. 2b). In a–c, the histograms show the distributions for v-goggled cats (vertical, n = 102; horizontal, n = 27; oblique, n = 17), whereas the curves show the distributions for normal cats (vertical, n = 63; horizontal, n = 54; oblique, n = 131). The number of cells was reduced for spatial frequency bandwidth to define the high cutoff frequency in both v-goggled (vertical, n = 98; horizontal, n = 26; oblique, n = 13) and normal cats (vertical, n = 57; horizontal, n = 51; oblique, n = 123). The colours indicate 3 groups based on the preferred orientation. The error bars in d–f indicate s.e.m. Horz, horizontal; obl, oblique. V, vertical; H, horizontal; O, oblique. **p < 0.01, ***p < 0.005, ****p < 0.001, Tukey-Kramer method for multiple comparisons after the Kruskal-Wallis test.
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f4: Orientation and spatial frequency tuning of single neurons.The orientation and spatial frequency tuning parameters of individual neurons were obtained by fitting a Gaussian function to the response surfaces of each cell (Fig. 2b). In a–c, the histograms show the distributions for v-goggled cats (vertical, n = 102; horizontal, n = 27; oblique, n = 17), whereas the curves show the distributions for normal cats (vertical, n = 63; horizontal, n = 54; oblique, n = 131). The number of cells was reduced for spatial frequency bandwidth to define the high cutoff frequency in both v-goggled (vertical, n = 98; horizontal, n = 26; oblique, n = 13) and normal cats (vertical, n = 57; horizontal, n = 51; oblique, n = 123). The colours indicate 3 groups based on the preferred orientation. The error bars in d–f indicate s.e.m. Horz, horizontal; obl, oblique. V, vertical; H, horizontal; O, oblique. **p < 0.01, ***p < 0.005, ****p < 0.001, Tukey-Kramer method for multiple comparisons after the Kruskal-Wallis test.

Mentions: Figure 4 summarises the orientation and spatial frequency tuning parameters of individual neurons in v-goggled and normal cats. In v-goggled cats, neurons tuned to the vertical orientation had a significantly narrower orientation tuning bandwidth (full width at half height) (27.6° ± 17.7° [mean ± s.d.], n = 102; Fig. 4a,d) than those tuned to the non-vertical orientations (52.6° ± 25.5°, n = 44; p < 0.001, Tukey-Kramer multiple-comparison test). More notably, orientation bandwidth for neurons tuned to the vertical orientation in v-goggled cats was narrower than that for cells in normal cats (40.5° ± 20.9°, n = 249; p < 0.001, Tukey-Kramer multiple-comparison test). Conversely, neurons tuned to the non-vertical orientation in v-goggled cats had a broader orientation bandwidth than that for cells in normal cats (p < 0.01, Tukey-Kramer multiple-comparison test).


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 and spatial frequency tuning of single neurons.The orientation and spatial frequency tuning parameters of individual neurons were obtained by fitting a Gaussian function to the response surfaces of each cell (Fig. 2b). In a–c, the histograms show the distributions for v-goggled cats (vertical, n = 102; horizontal, n = 27; oblique, n = 17), whereas the curves show the distributions for normal cats (vertical, n = 63; horizontal, n = 54; oblique, n = 131). The number of cells was reduced for spatial frequency bandwidth to define the high cutoff frequency in both v-goggled (vertical, n = 98; horizontal, n = 26; oblique, n = 13) and normal cats (vertical, n = 57; horizontal, n = 51; oblique, n = 123). The colours indicate 3 groups based on the preferred orientation. The error bars in d–f indicate s.e.m. Horz, horizontal; obl, oblique. V, vertical; H, horizontal; O, oblique. **p < 0.01, ***p < 0.005, ****p < 0.001, Tukey-Kramer method for multiple comparisons after the Kruskal-Wallis test.
© Copyright Policy - open-access
Related In: Results  -  Collection

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f4: Orientation and spatial frequency tuning of single neurons.The orientation and spatial frequency tuning parameters of individual neurons were obtained by fitting a Gaussian function to the response surfaces of each cell (Fig. 2b). In a–c, the histograms show the distributions for v-goggled cats (vertical, n = 102; horizontal, n = 27; oblique, n = 17), whereas the curves show the distributions for normal cats (vertical, n = 63; horizontal, n = 54; oblique, n = 131). The number of cells was reduced for spatial frequency bandwidth to define the high cutoff frequency in both v-goggled (vertical, n = 98; horizontal, n = 26; oblique, n = 13) and normal cats (vertical, n = 57; horizontal, n = 51; oblique, n = 123). The colours indicate 3 groups based on the preferred orientation. The error bars in d–f indicate s.e.m. Horz, horizontal; obl, oblique. V, vertical; H, horizontal; O, oblique. **p < 0.01, ***p < 0.005, ****p < 0.001, Tukey-Kramer method for multiple comparisons after the Kruskal-Wallis test.
Mentions: Figure 4 summarises the orientation and spatial frequency tuning parameters of individual neurons in v-goggled and normal cats. In v-goggled cats, neurons tuned to the vertical orientation had a significantly narrower orientation tuning bandwidth (full width at half height) (27.6° ± 17.7° [mean ± s.d.], n = 102; Fig. 4a,d) than those tuned to the non-vertical orientations (52.6° ± 25.5°, n = 44; p < 0.001, Tukey-Kramer multiple-comparison test). More notably, orientation bandwidth for neurons tuned to the vertical orientation in v-goggled cats was narrower than that for cells in normal cats (40.5° ± 20.9°, n = 249; p < 0.001, Tukey-Kramer multiple-comparison test). Conversely, neurons tuned to the non-vertical orientation in v-goggled cats had a broader orientation bandwidth than that for cells in normal cats (p < 0.01, Tukey-Kramer multiple-comparison test).

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.