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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.


Receptive fields and responses to gratings of different orientations and spatial frequencies for 3 neurons.Data for each cell are shown in separate columns. (a) Receptive fields were mapped by presenting a small optimal grating patch at various positions. Stimuli are shown to scale for each neuron in the upper right corner. Scale bars, 5°. (b) Two-dimensional tuning to orientation and spatial frequency was examined by presenting gratings of various orientation and spatial frequency combinations. The tuning surface is represented in polar coordinates common to all neurons to simplify comparisons (up to 1 cpd, the perimeter of the circular area). Spatial frequencies of the stimuli were spaced equally on a logarithmic scale, hence the coarser appearance at higher frequencies. The crosshairs denote the peak position of the Gaussian function fitted to the tuning surface (i.e., preferred orientation and spatial frequency), while the inner and outer ellipses indicate the contours at 50% and 10% peak values, respectively. The orientation bandwidth was defined using a 50% criterion, shown as the angle between the two radial grey lines.
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f2: Receptive fields and responses to gratings of different orientations and spatial frequencies for 3 neurons.Data for each cell are shown in separate columns. (a) Receptive fields were mapped by presenting a small optimal grating patch at various positions. Stimuli are shown to scale for each neuron in the upper right corner. Scale bars, 5°. (b) Two-dimensional tuning to orientation and spatial frequency was examined by presenting gratings of various orientation and spatial frequency combinations. The tuning surface is represented in polar coordinates common to all neurons to simplify comparisons (up to 1 cpd, the perimeter of the circular area). Spatial frequencies of the stimuli were spaced equally on a logarithmic scale, hence the coarser appearance at higher frequencies. The crosshairs denote the peak position of the Gaussian function fitted to the tuning surface (i.e., preferred orientation and spatial frequency), while the inner and outer ellipses indicate the contours at 50% and 10% peak values, respectively. The orientation bandwidth was defined using a 50% criterion, shown as the angle between the two radial grey lines.

Mentions: To study the effect of orientation-restricted rearing on various tuning properties of individual neurons, single unit activities were recorded using a pair of tungsten microelectrodes inserted into the primary visual cortex of anaesthetised and paralysed cats. Seventeen penetrations were made oblique to the cortical surface in three v-goggled cats. For comparison, the same set of data was also collected from three age-matched normal cats (17 oblique penetrations). Figure 2 shows the responses of representative neurons in v-goggled cats. The top panel (Fig. 2a) shows the overall shape of their receptive fields (i.e., tuning to spatial position) mapped by presenting small grating patches in various locations. Two neurons tuned to the vertical orientation (Fig. 2a, left and middle) exhibited vertically elongated receptive fields, whereas the third neuron tuned to the horizontal orientation (Fig. 2a, right) showed a round receptive field.


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)

Receptive fields and responses to gratings of different orientations and spatial frequencies for 3 neurons.Data for each cell are shown in separate columns. (a) Receptive fields were mapped by presenting a small optimal grating patch at various positions. Stimuli are shown to scale for each neuron in the upper right corner. Scale bars, 5°. (b) Two-dimensional tuning to orientation and spatial frequency was examined by presenting gratings of various orientation and spatial frequency combinations. The tuning surface is represented in polar coordinates common to all neurons to simplify comparisons (up to 1 cpd, the perimeter of the circular area). Spatial frequencies of the stimuli were spaced equally on a logarithmic scale, hence the coarser appearance at higher frequencies. The crosshairs denote the peak position of the Gaussian function fitted to the tuning surface (i.e., preferred orientation and spatial frequency), while the inner and outer ellipses indicate the contours at 50% and 10% peak values, respectively. The orientation bandwidth was defined using a 50% criterion, shown as the angle between the two radial grey lines.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f2: Receptive fields and responses to gratings of different orientations and spatial frequencies for 3 neurons.Data for each cell are shown in separate columns. (a) Receptive fields were mapped by presenting a small optimal grating patch at various positions. Stimuli are shown to scale for each neuron in the upper right corner. Scale bars, 5°. (b) Two-dimensional tuning to orientation and spatial frequency was examined by presenting gratings of various orientation and spatial frequency combinations. The tuning surface is represented in polar coordinates common to all neurons to simplify comparisons (up to 1 cpd, the perimeter of the circular area). Spatial frequencies of the stimuli were spaced equally on a logarithmic scale, hence the coarser appearance at higher frequencies. The crosshairs denote the peak position of the Gaussian function fitted to the tuning surface (i.e., preferred orientation and spatial frequency), while the inner and outer ellipses indicate the contours at 50% and 10% peak values, respectively. The orientation bandwidth was defined using a 50% criterion, shown as the angle between the two radial grey lines.
Mentions: To study the effect of orientation-restricted rearing on various tuning properties of individual neurons, single unit activities were recorded using a pair of tungsten microelectrodes inserted into the primary visual cortex of anaesthetised and paralysed cats. Seventeen penetrations were made oblique to the cortical surface in three v-goggled cats. For comparison, the same set of data was also collected from three age-matched normal cats (17 oblique penetrations). Figure 2 shows the responses of representative neurons in v-goggled cats. The top panel (Fig. 2a) shows the overall shape of their receptive fields (i.e., tuning to spatial position) mapped by presenting small grating patches in various locations. Two neurons tuned to the vertical orientation (Fig. 2a, left and middle) exhibited vertically elongated receptive fields, whereas the third neuron tuned to the horizontal orientation (Fig. 2a, right) showed a round receptive field.

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.