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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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Related in: MedlinePlus

Response of a representative cell.(A) Spatial relation between stimuli in screen coordinates (calibration bar = 1 deg). White cross represents fixation target, and the dashed circle (invisible to the animal) encloses the RF of the recorded neuron determined with a spatial summation test. Gabor stimulus at RF (S2) is at preferrred orientation. S1 was presented at one of four locations, a–d, along the axis orthogonal to that of RF orientation, with a spacing of one RF diameter. All S1 orientations were parallel to S2. There were 44 unique stimulus sequences (4 S1 positions×11 SOAs), plus five single stimulus conditions at each S1 and S2 locations. These 49 stimulus conditions were randomly repeated. (B) Raster and density plots of response to S1 at positions a–d aligned at its onset. Spike density function was derived by convolving spike sequence with an asymmetric kernel function [66]. Y-axis indicates spike density in spikes/s. Note that no S1 alone at positions a-d evoked spike response. (C) Raster and density plots for S2 alone and S1c-S2 sequence stimuli with SOAs of 30 and 50 ms chosen to illustrate response modulation. Trials are aligned at S2 onset. It can be seen that the magnitude of initial and sustained response varied with SOA. (D) An example SOA-time plot compiled from spike density for S1c-S2 sequence stimuli, the first stimulus at positions c and the second stimulus at RF. Y-axis is SOA, determined in 10-ms step. The times of S1 onset for each SOA condition are indicated as small white circles. Data are linearly interpolated across SOA. The S2-alone condition is given above for comparison. Note that the cell’s response varied with SOA. (E) Determination of significant modulation. Spike density curves for S2 alone (black) and S1c-S2 sequence with SOA of 80 ms (green), along with horizotal marks (top) of temporal epochs associated with statistically significant decrease (blue) and increase (red) from S2 alone condition. (F) Time course of significant modulation of spike response by sequence stimuli as shown in E. Spike density following S1–S2 sequence was compared with spike density following S2 for each of temporal epochs of 30 ms with a shift of 5 ms. The temporal epochs with a statistically-significant decrease in spike density as determined with Mann-Whitney U-test are shown in blue bars, and significant increase in red bars, centering on corresponding analysis windows, revealing the magnitude and time course of suppressive and facilitative effects of S1 that depend on S1 position and SOA. The dark symbols represent significant modulation at p<0.01, and the light ones are p<0.05.
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pone-0047543-g003: Response of a representative cell.(A) Spatial relation between stimuli in screen coordinates (calibration bar = 1 deg). White cross represents fixation target, and the dashed circle (invisible to the animal) encloses the RF of the recorded neuron determined with a spatial summation test. Gabor stimulus at RF (S2) is at preferrred orientation. S1 was presented at one of four locations, a–d, along the axis orthogonal to that of RF orientation, with a spacing of one RF diameter. All S1 orientations were parallel to S2. There were 44 unique stimulus sequences (4 S1 positions×11 SOAs), plus five single stimulus conditions at each S1 and S2 locations. These 49 stimulus conditions were randomly repeated. (B) Raster and density plots of response to S1 at positions a–d aligned at its onset. Spike density function was derived by convolving spike sequence with an asymmetric kernel function [66]. Y-axis indicates spike density in spikes/s. Note that no S1 alone at positions a-d evoked spike response. (C) Raster and density plots for S2 alone and S1c-S2 sequence stimuli with SOAs of 30 and 50 ms chosen to illustrate response modulation. Trials are aligned at S2 onset. It can be seen that the magnitude of initial and sustained response varied with SOA. (D) An example SOA-time plot compiled from spike density for S1c-S2 sequence stimuli, the first stimulus at positions c and the second stimulus at RF. Y-axis is SOA, determined in 10-ms step. The times of S1 onset for each SOA condition are indicated as small white circles. Data are linearly interpolated across SOA. The S2-alone condition is given above for comparison. Note that the cell’s response varied with SOA. (E) Determination of significant modulation. Spike density curves for S2 alone (black) and S1c-S2 sequence with SOA of 80 ms (green), along with horizotal marks (top) of temporal epochs associated with statistically significant decrease (blue) and increase (red) from S2 alone condition. (F) Time course of significant modulation of spike response by sequence stimuli as shown in E. Spike density following S1–S2 sequence was compared with spike density following S2 for each of temporal epochs of 30 ms with a shift of 5 ms. The temporal epochs with a statistically-significant decrease in spike density as determined with Mann-Whitney U-test are shown in blue bars, and significant increase in red bars, centering on corresponding analysis windows, revealing the magnitude and time course of suppressive and facilitative effects of S1 that depend on S1 position and SOA. The dark symbols represent significant modulation at p<0.01, and the light ones are p<0.05.

Mentions: Fig. 3 illustrates the activity of a representative V1 cell recorded during the task. For this cell, S1 was presented at one of four positions, a through d, along the axis perpendicular to the orientation of S2 (Fig. 3A). S1 alone evoked no spike responses at any of these four positions, verifying that these stimuli were presented outside the RF (Fig. 3B). In contrast, S2 alone evoked a vigorous spike response that started at around 50 ms, peaked at around 100 ms after S2 onset, and decayed thereafter (upper panel of Fig. 3C). When S1 and S2 were sequentially presented, S1 did modulate the cell’s response to S2 in a manner that varied with SOA. For example, when S1 was presented 30 ms prior to S2, the response became more sustained (middle panel of Fig. 3C), whereas with an SOA of 50 ms, the peak response was considerably reduced (lower panel of Fig. 3C).


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

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

Response of a representative cell.(A) Spatial relation between stimuli in screen coordinates (calibration bar = 1 deg). White cross represents fixation target, and the dashed circle (invisible to the animal) encloses the RF of the recorded neuron determined with a spatial summation test. Gabor stimulus at RF (S2) is at preferrred orientation. S1 was presented at one of four locations, a–d, along the axis orthogonal to that of RF orientation, with a spacing of one RF diameter. All S1 orientations were parallel to S2. There were 44 unique stimulus sequences (4 S1 positions×11 SOAs), plus five single stimulus conditions at each S1 and S2 locations. These 49 stimulus conditions were randomly repeated. (B) Raster and density plots of response to S1 at positions a–d aligned at its onset. Spike density function was derived by convolving spike sequence with an asymmetric kernel function [66]. Y-axis indicates spike density in spikes/s. Note that no S1 alone at positions a-d evoked spike response. (C) Raster and density plots for S2 alone and S1c-S2 sequence stimuli with SOAs of 30 and 50 ms chosen to illustrate response modulation. Trials are aligned at S2 onset. It can be seen that the magnitude of initial and sustained response varied with SOA. (D) An example SOA-time plot compiled from spike density for S1c-S2 sequence stimuli, the first stimulus at positions c and the second stimulus at RF. Y-axis is SOA, determined in 10-ms step. The times of S1 onset for each SOA condition are indicated as small white circles. Data are linearly interpolated across SOA. The S2-alone condition is given above for comparison. Note that the cell’s response varied with SOA. (E) Determination of significant modulation. Spike density curves for S2 alone (black) and S1c-S2 sequence with SOA of 80 ms (green), along with horizotal marks (top) of temporal epochs associated with statistically significant decrease (blue) and increase (red) from S2 alone condition. (F) Time course of significant modulation of spike response by sequence stimuli as shown in E. Spike density following S1–S2 sequence was compared with spike density following S2 for each of temporal epochs of 30 ms with a shift of 5 ms. The temporal epochs with a statistically-significant decrease in spike density as determined with Mann-Whitney U-test are shown in blue bars, and significant increase in red bars, centering on corresponding analysis windows, revealing the magnitude and time course of suppressive and facilitative effects of S1 that depend on S1 position and SOA. The dark symbols represent significant modulation at p<0.01, and the light ones are p<0.05.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3472985&req=5

pone-0047543-g003: Response of a representative cell.(A) Spatial relation between stimuli in screen coordinates (calibration bar = 1 deg). White cross represents fixation target, and the dashed circle (invisible to the animal) encloses the RF of the recorded neuron determined with a spatial summation test. Gabor stimulus at RF (S2) is at preferrred orientation. S1 was presented at one of four locations, a–d, along the axis orthogonal to that of RF orientation, with a spacing of one RF diameter. All S1 orientations were parallel to S2. There were 44 unique stimulus sequences (4 S1 positions×11 SOAs), plus five single stimulus conditions at each S1 and S2 locations. These 49 stimulus conditions were randomly repeated. (B) Raster and density plots of response to S1 at positions a–d aligned at its onset. Spike density function was derived by convolving spike sequence with an asymmetric kernel function [66]. Y-axis indicates spike density in spikes/s. Note that no S1 alone at positions a-d evoked spike response. (C) Raster and density plots for S2 alone and S1c-S2 sequence stimuli with SOAs of 30 and 50 ms chosen to illustrate response modulation. Trials are aligned at S2 onset. It can be seen that the magnitude of initial and sustained response varied with SOA. (D) An example SOA-time plot compiled from spike density for S1c-S2 sequence stimuli, the first stimulus at positions c and the second stimulus at RF. Y-axis is SOA, determined in 10-ms step. The times of S1 onset for each SOA condition are indicated as small white circles. Data are linearly interpolated across SOA. The S2-alone condition is given above for comparison. Note that the cell’s response varied with SOA. (E) Determination of significant modulation. Spike density curves for S2 alone (black) and S1c-S2 sequence with SOA of 80 ms (green), along with horizotal marks (top) of temporal epochs associated with statistically significant decrease (blue) and increase (red) from S2 alone condition. (F) Time course of significant modulation of spike response by sequence stimuli as shown in E. Spike density following S1–S2 sequence was compared with spike density following S2 for each of temporal epochs of 30 ms with a shift of 5 ms. The temporal epochs with a statistically-significant decrease in spike density as determined with Mann-Whitney U-test are shown in blue bars, and significant increase in red bars, centering on corresponding analysis windows, revealing the magnitude and time course of suppressive and facilitative effects of S1 that depend on S1 position and SOA. The dark symbols represent significant modulation at p<0.01, and the light ones are p<0.05.
Mentions: Fig. 3 illustrates the activity of a representative V1 cell recorded during the task. For this cell, S1 was presented at one of four positions, a through d, along the axis perpendicular to the orientation of S2 (Fig. 3A). S1 alone evoked no spike responses at any of these four positions, verifying that these stimuli were presented outside the RF (Fig. 3B). In contrast, S2 alone evoked a vigorous spike response that started at around 50 ms, peaked at around 100 ms after S2 onset, and decayed thereafter (upper panel of Fig. 3C). When S1 and S2 were sequentially presented, S1 did modulate the cell’s response to S2 in a manner that varied with SOA. For example, when S1 was presented 30 ms prior to S2, the response became more sustained (middle panel of Fig. 3C), whereas with an SOA of 50 ms, the peak response was considerably reduced (lower panel of Fig. 3C).

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