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Modulation of V1 spike response by temporal interval of spatiotemporal stimulus sequence.

Kim T, Kim HR, Kim K, Lee C - PLoS ONE (2012)

Bottom Line: The spike activity of single neurons of the primary visual cortex (V1) becomes more selective and reliable in response to wide-field natural scenes compared to smaller stimuli confined to the classical receptive field (RF).This stimulus configuration enabled us to examine the spatiotemporal selectivity of response modulation from a focal surround region.These results suggest that V1 neurons participate in processing spatiotemporal sequences of oriented stimuli extending outside the RF.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, Seoul National University, Kwanak, Seoul, Korea.

ABSTRACT
The spike activity of single neurons of the primary visual cortex (V1) becomes more selective and reliable in response to wide-field natural scenes compared to smaller stimuli confined to the classical receptive field (RF). However, it is largely unknown what aspects of natural scenes increase the selectivity of V1 neurons. One hypothesis is that modulation by surround interaction is highly sensitive to small changes in spatiotemporal aspects of RF surround. Such a fine-tuned modulation would enable single neurons to hold information about spatiotemporal sequences of oriented stimuli, which extends the role of V1 neurons as a simple spatiotemporal filter confined to the RF. In the current study, we examined the hypothesis in the V1 of awake behaving monkeys, by testing whether the spike response of single V1 neurons is modulated by temporal interval of spatiotemporal stimulus sequence encompassing inside and outside the RF. We used two identical Gabor stimuli that were sequentially presented with a variable stimulus onset asynchrony (SOA): the preceding one (S1) outside the RF and the following one (S2) in the RF. This stimulus configuration enabled us to examine the spatiotemporal selectivity of response modulation from a focal surround region. Although S1 alone did not evoke spike responses, visual response to S2 was modulated for SOA in the range of tens of milliseconds. These results suggest that V1 neurons participate in processing spatiotemporal sequences of oriented stimuli extending outside the RF.

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Periodic SOA-dependency of surround modulation.(A) Modulation of spike response in percentage as a function of SOA for three S1 locations of Fig. 5; green: a, blue: b, red: c. (B) Periodic component. The best fit linear trend was removed from the spline fit of modulation percentage in A for each S1 position to remove the monotonic component (detrend.m provided by the MATLAB). (C) The auto-correlogram (black) of the detrended modulation of S1a (green curve of B) was fit with a cosine-Gaussian function,  (gray). (D) Hstogram of periodicity. Each case is the first non-zero peak of a cosine-Gaussian function, taken from 53 out of 276 stimulus conditions, for which the cosine-Gaussian fit explained more than 90% variance of auto-correlation curve. For three examples of B, R-squares are 0.99 (S1a), 0.94 (S1b), 0.99 (S1c). The mean periodicity of 53 stimulus conditions is 36.62 ms. (E) Cross-correlation between detrended green and blue curves of B. The time lag at the maximum cross-correlation is 20 ms. This lag reflects the distance between S1a (green) and S1b (blue). Given that cortical distance between S1a and S1b was 3.07 mm, the propagation speed in this example is estimated to be 0.15 m/s. (F) Histogram of propagation speed. Shown is propagation speed for each of 30 cases in which at least one S1 position passed the periodicity criteria of C. The mean distribution is 0.14 m/s without 3 outliers. The median is 0.11 m/s.
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pone-0047543-g006: Periodic SOA-dependency of surround modulation.(A) Modulation of spike response in percentage as a function of SOA for three S1 locations of Fig. 5; green: a, blue: b, red: c. (B) Periodic component. The best fit linear trend was removed from the spline fit of modulation percentage in A for each S1 position to remove the monotonic component (detrend.m provided by the MATLAB). (C) The auto-correlogram (black) of the detrended modulation of S1a (green curve of B) was fit with a cosine-Gaussian function, (gray). (D) Hstogram of periodicity. Each case is the first non-zero peak of a cosine-Gaussian function, taken from 53 out of 276 stimulus conditions, for which the cosine-Gaussian fit explained more than 90% variance of auto-correlation curve. For three examples of B, R-squares are 0.99 (S1a), 0.94 (S1b), 0.99 (S1c). The mean periodicity of 53 stimulus conditions is 36.62 ms. (E) Cross-correlation between detrended green and blue curves of B. The time lag at the maximum cross-correlation is 20 ms. This lag reflects the distance between S1a (green) and S1b (blue). Given that cortical distance between S1a and S1b was 3.07 mm, the propagation speed in this example is estimated to be 0.15 m/s. (F) Histogram of propagation speed. Shown is propagation speed for each of 30 cases in which at least one S1 position passed the periodicity criteria of C. The mean distribution is 0.14 m/s without 3 outliers. The median is 0.11 m/s.

Mentions: The response to S2 was often modulated at periodic SOAs. Fig. 6A illustrates an example of periodic SOA-dependency of response modulation, taken from the cell of Fig. 5. The suppressive modulation in Fig. 6A appears to be consisted of two components; a monotonic and a periodic SOA-dependencies. A monotonic component depends on the spatial proximity of S1 to S2 and on SOA between them. The suppressive modulation for the cell was larger with a closer S1 and at shorter SOAs; compare overall vertical positions of green, blue, and red traces, and compare modulation magnitude between shorter and longer SOAs. In addition to this monotonic component, response modulation was repetitive at multiple SOAs, and appears to be periodic. To quantify the periodic component, the linear trend was first removed (Fig. 6B), and the auto-correlation of the detrended function was fitted with a cosine-Gaussian function (Fig. 6C). The periodicity was taken from the fitted cosine-Gaussian function that explained more than 90% of variance of the auto-correlation function. The mean periodicity of 53 out of 276 stimulus conditions for 45 recording sites (14 single-units and 31 multiple-units) was 36.62 ms (Fig. 6D). This indicates that for these conditions the influence from focal surround regions arrives in a repetitive wave of gamma frequency. This may be related to the fact that stimulus onset generates a neural response in a gamma rhythm [26], [27] based on a network of inhibitory interneurons [28], [29] that propagates and results in modulation of spike response in a gamma rhythm [30].


Modulation of V1 spike response by temporal interval of spatiotemporal stimulus sequence.

Kim T, Kim HR, Kim K, Lee C - PLoS ONE (2012)

Periodic SOA-dependency of surround modulation.(A) Modulation of spike response in percentage as a function of SOA for three S1 locations of Fig. 5; green: a, blue: b, red: c. (B) Periodic component. The best fit linear trend was removed from the spline fit of modulation percentage in A for each S1 position to remove the monotonic component (detrend.m provided by the MATLAB). (C) The auto-correlogram (black) of the detrended modulation of S1a (green curve of B) was fit with a cosine-Gaussian function,  (gray). (D) Hstogram of periodicity. Each case is the first non-zero peak of a cosine-Gaussian function, taken from 53 out of 276 stimulus conditions, for which the cosine-Gaussian fit explained more than 90% variance of auto-correlation curve. For three examples of B, R-squares are 0.99 (S1a), 0.94 (S1b), 0.99 (S1c). The mean periodicity of 53 stimulus conditions is 36.62 ms. (E) Cross-correlation between detrended green and blue curves of B. The time lag at the maximum cross-correlation is 20 ms. This lag reflects the distance between S1a (green) and S1b (blue). Given that cortical distance between S1a and S1b was 3.07 mm, the propagation speed in this example is estimated to be 0.15 m/s. (F) Histogram of propagation speed. Shown is propagation speed for each of 30 cases in which at least one S1 position passed the periodicity criteria of C. The mean distribution is 0.14 m/s without 3 outliers. The median is 0.11 m/s.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3472985&req=5

pone-0047543-g006: Periodic SOA-dependency of surround modulation.(A) Modulation of spike response in percentage as a function of SOA for three S1 locations of Fig. 5; green: a, blue: b, red: c. (B) Periodic component. The best fit linear trend was removed from the spline fit of modulation percentage in A for each S1 position to remove the monotonic component (detrend.m provided by the MATLAB). (C) The auto-correlogram (black) of the detrended modulation of S1a (green curve of B) was fit with a cosine-Gaussian function, (gray). (D) Hstogram of periodicity. Each case is the first non-zero peak of a cosine-Gaussian function, taken from 53 out of 276 stimulus conditions, for which the cosine-Gaussian fit explained more than 90% variance of auto-correlation curve. For three examples of B, R-squares are 0.99 (S1a), 0.94 (S1b), 0.99 (S1c). The mean periodicity of 53 stimulus conditions is 36.62 ms. (E) Cross-correlation between detrended green and blue curves of B. The time lag at the maximum cross-correlation is 20 ms. This lag reflects the distance between S1a (green) and S1b (blue). Given that cortical distance between S1a and S1b was 3.07 mm, the propagation speed in this example is estimated to be 0.15 m/s. (F) Histogram of propagation speed. Shown is propagation speed for each of 30 cases in which at least one S1 position passed the periodicity criteria of C. The mean distribution is 0.14 m/s without 3 outliers. The median is 0.11 m/s.
Mentions: The response to S2 was often modulated at periodic SOAs. Fig. 6A illustrates an example of periodic SOA-dependency of response modulation, taken from the cell of Fig. 5. The suppressive modulation in Fig. 6A appears to be consisted of two components; a monotonic and a periodic SOA-dependencies. A monotonic component depends on the spatial proximity of S1 to S2 and on SOA between them. The suppressive modulation for the cell was larger with a closer S1 and at shorter SOAs; compare overall vertical positions of green, blue, and red traces, and compare modulation magnitude between shorter and longer SOAs. In addition to this monotonic component, response modulation was repetitive at multiple SOAs, and appears to be periodic. To quantify the periodic component, the linear trend was first removed (Fig. 6B), and the auto-correlation of the detrended function was fitted with a cosine-Gaussian function (Fig. 6C). The periodicity was taken from the fitted cosine-Gaussian function that explained more than 90% of variance of the auto-correlation function. The mean periodicity of 53 out of 276 stimulus conditions for 45 recording sites (14 single-units and 31 multiple-units) was 36.62 ms (Fig. 6D). This indicates that for these conditions the influence from focal surround regions arrives in a repetitive wave of gamma frequency. This may be related to the fact that stimulus onset generates a neural response in a gamma rhythm [26], [27] based on a network of inhibitory interneurons [28], [29] that propagates and results in modulation of spike response in a gamma rhythm [30].

Bottom Line: The spike activity of single neurons of the primary visual cortex (V1) becomes more selective and reliable in response to wide-field natural scenes compared to smaller stimuli confined to the classical receptive field (RF).This stimulus configuration enabled us to examine the spatiotemporal selectivity of response modulation from a focal surround region.These results suggest that V1 neurons participate in processing spatiotemporal sequences of oriented stimuli extending outside the RF.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, Seoul National University, Kwanak, Seoul, Korea.

ABSTRACT
The spike activity of single neurons of the primary visual cortex (V1) becomes more selective and reliable in response to wide-field natural scenes compared to smaller stimuli confined to the classical receptive field (RF). However, it is largely unknown what aspects of natural scenes increase the selectivity of V1 neurons. One hypothesis is that modulation by surround interaction is highly sensitive to small changes in spatiotemporal aspects of RF surround. Such a fine-tuned modulation would enable single neurons to hold information about spatiotemporal sequences of oriented stimuli, which extends the role of V1 neurons as a simple spatiotemporal filter confined to the RF. In the current study, we examined the hypothesis in the V1 of awake behaving monkeys, by testing whether the spike response of single V1 neurons is modulated by temporal interval of spatiotemporal stimulus sequence encompassing inside and outside the RF. We used two identical Gabor stimuli that were sequentially presented with a variable stimulus onset asynchrony (SOA): the preceding one (S1) outside the RF and the following one (S2) in the RF. This stimulus configuration enabled us to examine the spatiotemporal selectivity of response modulation from a focal surround region. Although S1 alone did not evoke spike responses, visual response to S2 was modulated for SOA in the range of tens of milliseconds. These results suggest that V1 neurons participate in processing spatiotemporal sequences of oriented stimuli extending outside the RF.

Show MeSH
Related in: MedlinePlus