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Neuronal basis of perceptual learning in striate cortex.

Ren Z, Zhou J, Yao Z, Wang Z, Yuan N, Xu G, Wang X, Zhang B, Hess RF, Zhou Y - Sci Rep (2016)

Bottom Line: It is well known that, in humans, contrast sensitivity training at high spatial frequency (SF) not only leads to contrast sensitivity improvement, but also results in an improvement in visual acuity as assessed with gratings (direct effect) or letters (transfer effect).Furthermore, both the neuronal differences in OSF and SNR were significantly correlated with the improvement of acuity measured behaviorally.These results suggest that striate neurons might mediate the perceptual learning-induced improvement for high spatial frequency stimuli by an alteration in their spatial frequency representation and by an increased SNR.

View Article: PubMed Central - PubMed

Affiliation: CAS Key Laboratory of Brain Function and Disease, and School of Life Sciences, University of Science and Technology of China, Hefei, Anhui, P.R. China.

ABSTRACT
It is well known that, in humans, contrast sensitivity training at high spatial frequency (SF) not only leads to contrast sensitivity improvement, but also results in an improvement in visual acuity as assessed with gratings (direct effect) or letters (transfer effect). However, the underlying neural mechanisms of this high spatial frequency training improvement remain to be elucidated. In the present study, we examined four properties of neurons in primary visual cortex (area 17) of adult cats that exhibited significantly improved acuity after contrast sensitivity training with a high spatial frequency grating and those of untrained control cats. We found no difference in neuronal contrast sensitivity or tuning width (Width) between the trained and untrained cats. However, the trained cats showed a displacement of the cells' optimal spatial frequency (OSF) to higher spatial frequencies as well as a larger neuronal signal-to-noise ratio (SNR). Furthermore, both the neuronal differences in OSF and SNR were significantly correlated with the improvement of acuity measured behaviorally. These results suggest that striate neurons might mediate the perceptual learning-induced improvement for high spatial frequency stimuli by an alteration in their spatial frequency representation and by an increased SNR.

No MeSH data available.


Related in: MedlinePlus

Possible changes in neuronal SF tuning after training and schematic diagram of apparatus for training cats.(a) Possible mechanisms in neuronal SF tuning underlying the visual acuity improvement. (1) Increase of optimal spatial frequency (OSF). Learning may increase the number of cells in the cortical population that prefer the trained SF, which means that the OSF of neurons in the trained cats would shift to spatial frequencies matching the trained spatial frequency. (2) Increase in tuning width (Width). Training may increase Width so that the response to the high SF increases. (3) Improvement of signal-to-noise ratio (SNR). SNR is defined as Rmax (fitted maximal visually evoked response)/M (measured spontaneous activity). Learning may lead to an increase of Rmax and/or a decrease of M, which result in an increase in SNR. (b) Cats were trained monocularly to walk through a box and jumped onto the glass above a monitor on which two orthogonal stimuli were displayed. Jumps to the vertical one were rewarded with food and petting, whereas the horizontal one resulted in denial of the rewards and immediate next trial. In the training stage, frequency of the grating was relatively high and remained unchanged for each cat. A staircase procedure was used to track the threshold contrast of the grating for each cat over the entire training course. Visual acuities (grating acuities) of the two eyes were measured before and after the training stage.
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f1: Possible changes in neuronal SF tuning after training and schematic diagram of apparatus for training cats.(a) Possible mechanisms in neuronal SF tuning underlying the visual acuity improvement. (1) Increase of optimal spatial frequency (OSF). Learning may increase the number of cells in the cortical population that prefer the trained SF, which means that the OSF of neurons in the trained cats would shift to spatial frequencies matching the trained spatial frequency. (2) Increase in tuning width (Width). Training may increase Width so that the response to the high SF increases. (3) Improvement of signal-to-noise ratio (SNR). SNR is defined as Rmax (fitted maximal visually evoked response)/M (measured spontaneous activity). Learning may lead to an increase of Rmax and/or a decrease of M, which result in an increase in SNR. (b) Cats were trained monocularly to walk through a box and jumped onto the glass above a monitor on which two orthogonal stimuli were displayed. Jumps to the vertical one were rewarded with food and petting, whereas the horizontal one resulted in denial of the rewards and immediate next trial. In the training stage, frequency of the grating was relatively high and remained unchanged for each cat. A staircase procedure was used to track the threshold contrast of the grating for each cat over the entire training course. Visual acuities (grating acuities) of the two eyes were measured before and after the training stage.

Mentions: Extensive training improves the performance on the trained feature, a phenomena which is known as perceptual learning. It has been well accepted that this occurs through the enhancement of the modulation in neuronal tuning to stimulus components that are relevant to the task1. Moreover, the learning effects transfer to stimuli other than the trained stimulus in some cases. Of the particular interest is the report that contrast sensitivity training at a high spatial frequency (SF) results not only in improvements of contrast sensitivity at the trained frequency, but also improvements in acuity for both gratings and letters234. While it is known that improved neuronal contrast sensitivity offers an explanation for the improvements in behavioral contrast sensitivity induced by perceptual learning at low spatial frequencies5 where acuity is unaffected, little is known of the neural basis of the perceptual learning effects for high spatial frequencies where acuity is also improved. Here we consider four possible neural explanations for the direct and transferred improvements found following perceptual learning at high spatial frequencies: 1) increase of the average contrast sensitivity of neurons tuned to high spatial frequencies6; 2) increase in the number of neurons responding to high spatial frequencies789, which shows as increased optimal spatial frequency (OSF) (Fig. 1a); 3) a broadening of the spatial frequency tuning response of individual neurons, which increases the response at high spatial frequencies (Fig. 1a), and 4) improved neuronal signal/noise ratio (SNR; Fig. 1a), in which maximal responses (Rmax) for high spatial frequency stimuli increased and/or spontaneous activity (M) decreased.


Neuronal basis of perceptual learning in striate cortex.

Ren Z, Zhou J, Yao Z, Wang Z, Yuan N, Xu G, Wang X, Zhang B, Hess RF, Zhou Y - Sci Rep (2016)

Possible changes in neuronal SF tuning after training and schematic diagram of apparatus for training cats.(a) Possible mechanisms in neuronal SF tuning underlying the visual acuity improvement. (1) Increase of optimal spatial frequency (OSF). Learning may increase the number of cells in the cortical population that prefer the trained SF, which means that the OSF of neurons in the trained cats would shift to spatial frequencies matching the trained spatial frequency. (2) Increase in tuning width (Width). Training may increase Width so that the response to the high SF increases. (3) Improvement of signal-to-noise ratio (SNR). SNR is defined as Rmax (fitted maximal visually evoked response)/M (measured spontaneous activity). Learning may lead to an increase of Rmax and/or a decrease of M, which result in an increase in SNR. (b) Cats were trained monocularly to walk through a box and jumped onto the glass above a monitor on which two orthogonal stimuli were displayed. Jumps to the vertical one were rewarded with food and petting, whereas the horizontal one resulted in denial of the rewards and immediate next trial. In the training stage, frequency of the grating was relatively high and remained unchanged for each cat. A staircase procedure was used to track the threshold contrast of the grating for each cat over the entire training course. Visual acuities (grating acuities) of the two eyes were measured before and after the training stage.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4837366&req=5

f1: Possible changes in neuronal SF tuning after training and schematic diagram of apparatus for training cats.(a) Possible mechanisms in neuronal SF tuning underlying the visual acuity improvement. (1) Increase of optimal spatial frequency (OSF). Learning may increase the number of cells in the cortical population that prefer the trained SF, which means that the OSF of neurons in the trained cats would shift to spatial frequencies matching the trained spatial frequency. (2) Increase in tuning width (Width). Training may increase Width so that the response to the high SF increases. (3) Improvement of signal-to-noise ratio (SNR). SNR is defined as Rmax (fitted maximal visually evoked response)/M (measured spontaneous activity). Learning may lead to an increase of Rmax and/or a decrease of M, which result in an increase in SNR. (b) Cats were trained monocularly to walk through a box and jumped onto the glass above a monitor on which two orthogonal stimuli were displayed. Jumps to the vertical one were rewarded with food and petting, whereas the horizontal one resulted in denial of the rewards and immediate next trial. In the training stage, frequency of the grating was relatively high and remained unchanged for each cat. A staircase procedure was used to track the threshold contrast of the grating for each cat over the entire training course. Visual acuities (grating acuities) of the two eyes were measured before and after the training stage.
Mentions: Extensive training improves the performance on the trained feature, a phenomena which is known as perceptual learning. It has been well accepted that this occurs through the enhancement of the modulation in neuronal tuning to stimulus components that are relevant to the task1. Moreover, the learning effects transfer to stimuli other than the trained stimulus in some cases. Of the particular interest is the report that contrast sensitivity training at a high spatial frequency (SF) results not only in improvements of contrast sensitivity at the trained frequency, but also improvements in acuity for both gratings and letters234. While it is known that improved neuronal contrast sensitivity offers an explanation for the improvements in behavioral contrast sensitivity induced by perceptual learning at low spatial frequencies5 where acuity is unaffected, little is known of the neural basis of the perceptual learning effects for high spatial frequencies where acuity is also improved. Here we consider four possible neural explanations for the direct and transferred improvements found following perceptual learning at high spatial frequencies: 1) increase of the average contrast sensitivity of neurons tuned to high spatial frequencies6; 2) increase in the number of neurons responding to high spatial frequencies789, which shows as increased optimal spatial frequency (OSF) (Fig. 1a); 3) a broadening of the spatial frequency tuning response of individual neurons, which increases the response at high spatial frequencies (Fig. 1a), and 4) improved neuronal signal/noise ratio (SNR; Fig. 1a), in which maximal responses (Rmax) for high spatial frequency stimuli increased and/or spontaneous activity (M) decreased.

Bottom Line: It is well known that, in humans, contrast sensitivity training at high spatial frequency (SF) not only leads to contrast sensitivity improvement, but also results in an improvement in visual acuity as assessed with gratings (direct effect) or letters (transfer effect).Furthermore, both the neuronal differences in OSF and SNR were significantly correlated with the improvement of acuity measured behaviorally.These results suggest that striate neurons might mediate the perceptual learning-induced improvement for high spatial frequency stimuli by an alteration in their spatial frequency representation and by an increased SNR.

View Article: PubMed Central - PubMed

Affiliation: CAS Key Laboratory of Brain Function and Disease, and School of Life Sciences, University of Science and Technology of China, Hefei, Anhui, P.R. China.

ABSTRACT
It is well known that, in humans, contrast sensitivity training at high spatial frequency (SF) not only leads to contrast sensitivity improvement, but also results in an improvement in visual acuity as assessed with gratings (direct effect) or letters (transfer effect). However, the underlying neural mechanisms of this high spatial frequency training improvement remain to be elucidated. In the present study, we examined four properties of neurons in primary visual cortex (area 17) of adult cats that exhibited significantly improved acuity after contrast sensitivity training with a high spatial frequency grating and those of untrained control cats. We found no difference in neuronal contrast sensitivity or tuning width (Width) between the trained and untrained cats. However, the trained cats showed a displacement of the cells' optimal spatial frequency (OSF) to higher spatial frequencies as well as a larger neuronal signal-to-noise ratio (SNR). Furthermore, both the neuronal differences in OSF and SNR were significantly correlated with the improvement of acuity measured behaviorally. These results suggest that striate neurons might mediate the perceptual learning-induced improvement for high spatial frequency stimuli by an alteration in their spatial frequency representation and by an increased SNR.

No MeSH data available.


Related in: MedlinePlus