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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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Pattern of modulation for collinear (A–D) and parallel (E–H) S1 conditions.(A) Combined time course of SOA-dependent significant facilitation (p<0.05) from 2288 SOA conditions of 208 collinear S1 stimuli. Normalized frequency of significant epoch is color-coded according to the color map shown on the right. Out of 2288, 208 (9.09%) SOA conditions included more than one temporal epoch with significant facilitation. (B) Time course of significant suppression combined from the same collinear S1 configurations. In 611 of 2288 (26.70%) SOA conditions, more than one temporal epoch showed significant suppression. (C) Normalized marginal frequency of significant facilitation from A (red) and suppression from B (blue) against peristimulus time. (D) Normalized marginal frequency of significant facilitation (A, red) and suppression (B, blue) during the poststimulus time period from 0 to 300 ms against SOA. Normallized marginal frequency was derived from marginal sum divided by the number of data points. (E–H) Similar plots as A–D combined from 572 SOA conditions of 52 parallel configurations. Out of 572 SOA conditions, 96 (16.78%) and 71 (12.41%) SOA groups showed significant facilitation and suppression, respectively. Thus, suppression was relatively common with collinear S1, and the relative ratio of facilitative modulation was higher with the parallel configuration. This was true even after the distance between S1 and S2 was taken into account (by subdividing S1 configuration conditions into two distance groups, one or two RF diameter away from RF center). Note that suppressive modulation was concentrated at around 100 ms after S2 onset time (C, G), whereas facilitative modulation was relatively more dispersed and dominant after around 200 ms after S2 onset, especially in the parallel configuration. Also note that collinear S1 tended to suppress at short SOA and facilitate at long SOA (D), whereas this dissociation was relatively weak with parallel S1 (H).
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pone-0047543-g008: Pattern of modulation for collinear (A–D) and parallel (E–H) S1 conditions.(A) Combined time course of SOA-dependent significant facilitation (p<0.05) from 2288 SOA conditions of 208 collinear S1 stimuli. Normalized frequency of significant epoch is color-coded according to the color map shown on the right. Out of 2288, 208 (9.09%) SOA conditions included more than one temporal epoch with significant facilitation. (B) Time course of significant suppression combined from the same collinear S1 configurations. In 611 of 2288 (26.70%) SOA conditions, more than one temporal epoch showed significant suppression. (C) Normalized marginal frequency of significant facilitation from A (red) and suppression from B (blue) against peristimulus time. (D) Normalized marginal frequency of significant facilitation (A, red) and suppression (B, blue) during the poststimulus time period from 0 to 300 ms against SOA. Normallized marginal frequency was derived from marginal sum divided by the number of data points. (E–H) Similar plots as A–D combined from 572 SOA conditions of 52 parallel configurations. Out of 572 SOA conditions, 96 (16.78%) and 71 (12.41%) SOA groups showed significant facilitation and suppression, respectively. Thus, suppression was relatively common with collinear S1, and the relative ratio of facilitative modulation was higher with the parallel configuration. This was true even after the distance between S1 and S2 was taken into account (by subdividing S1 configuration conditions into two distance groups, one or two RF diameter away from RF center). Note that suppressive modulation was concentrated at around 100 ms after S2 onset time (C, G), whereas facilitative modulation was relatively more dispersed and dominant after around 200 ms after S2 onset, especially in the parallel configuration. Also note that collinear S1 tended to suppress at short SOA and facilitate at long SOA (D), whereas this dissociation was relatively weak with parallel S1 (H).

Mentions: The sign of surround interaction is known to vary with stimulus contrast [10], [34]. Thus, the precise ratio of facilitative to suppressive interaction may vary. We focus here on the temporal interval rather than the sign of surround interaction, whether or not the incidence of significant suppression or facilitation is constant across SOA. For this, we combined the plots of the time course of SOA-dependent significant modulation, such as Fig. 3F, for suppression and facilitation separately for 260 experimental conditions in which the response to both S1–S2 sequence and S2 alone were tested (Fig. 8). Here again, it can be seen that for collinear S1 conditions, the incidence of significant suppression (Fig. 8B) was much more frequent than that of significant facilitation (Fig. 8A). This difference is not apparent for parallel S1 conditions (compare Fig. 8E and F). The time course of modulation was also different; for collinear S1 conditions, suppressive modulation was concentrated at around 100 ms after S2 onset (Fig. 8C), which corresponded to the time of peak response to S2 alone, whereas facilitative modulation was relatively more dispersed (Fig. 8E). For parallel S1 conditions, facilitation was dominant after about 200 ms following S2 onset.


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

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

Pattern of modulation for collinear (A–D) and parallel (E–H) S1 conditions.(A) Combined time course of SOA-dependent significant facilitation (p<0.05) from 2288 SOA conditions of 208 collinear S1 stimuli. Normalized frequency of significant epoch is color-coded according to the color map shown on the right. Out of 2288, 208 (9.09%) SOA conditions included more than one temporal epoch with significant facilitation. (B) Time course of significant suppression combined from the same collinear S1 configurations. In 611 of 2288 (26.70%) SOA conditions, more than one temporal epoch showed significant suppression. (C) Normalized marginal frequency of significant facilitation from A (red) and suppression from B (blue) against peristimulus time. (D) Normalized marginal frequency of significant facilitation (A, red) and suppression (B, blue) during the poststimulus time period from 0 to 300 ms against SOA. Normallized marginal frequency was derived from marginal sum divided by the number of data points. (E–H) Similar plots as A–D combined from 572 SOA conditions of 52 parallel configurations. Out of 572 SOA conditions, 96 (16.78%) and 71 (12.41%) SOA groups showed significant facilitation and suppression, respectively. Thus, suppression was relatively common with collinear S1, and the relative ratio of facilitative modulation was higher with the parallel configuration. This was true even after the distance between S1 and S2 was taken into account (by subdividing S1 configuration conditions into two distance groups, one or two RF diameter away from RF center). Note that suppressive modulation was concentrated at around 100 ms after S2 onset time (C, G), whereas facilitative modulation was relatively more dispersed and dominant after around 200 ms after S2 onset, especially in the parallel configuration. Also note that collinear S1 tended to suppress at short SOA and facilitate at long SOA (D), whereas this dissociation was relatively weak with parallel S1 (H).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3472985&req=5

pone-0047543-g008: Pattern of modulation for collinear (A–D) and parallel (E–H) S1 conditions.(A) Combined time course of SOA-dependent significant facilitation (p<0.05) from 2288 SOA conditions of 208 collinear S1 stimuli. Normalized frequency of significant epoch is color-coded according to the color map shown on the right. Out of 2288, 208 (9.09%) SOA conditions included more than one temporal epoch with significant facilitation. (B) Time course of significant suppression combined from the same collinear S1 configurations. In 611 of 2288 (26.70%) SOA conditions, more than one temporal epoch showed significant suppression. (C) Normalized marginal frequency of significant facilitation from A (red) and suppression from B (blue) against peristimulus time. (D) Normalized marginal frequency of significant facilitation (A, red) and suppression (B, blue) during the poststimulus time period from 0 to 300 ms against SOA. Normallized marginal frequency was derived from marginal sum divided by the number of data points. (E–H) Similar plots as A–D combined from 572 SOA conditions of 52 parallel configurations. Out of 572 SOA conditions, 96 (16.78%) and 71 (12.41%) SOA groups showed significant facilitation and suppression, respectively. Thus, suppression was relatively common with collinear S1, and the relative ratio of facilitative modulation was higher with the parallel configuration. This was true even after the distance between S1 and S2 was taken into account (by subdividing S1 configuration conditions into two distance groups, one or two RF diameter away from RF center). Note that suppressive modulation was concentrated at around 100 ms after S2 onset time (C, G), whereas facilitative modulation was relatively more dispersed and dominant after around 200 ms after S2 onset, especially in the parallel configuration. Also note that collinear S1 tended to suppress at short SOA and facilitate at long SOA (D), whereas this dissociation was relatively weak with parallel S1 (H).
Mentions: The sign of surround interaction is known to vary with stimulus contrast [10], [34]. Thus, the precise ratio of facilitative to suppressive interaction may vary. We focus here on the temporal interval rather than the sign of surround interaction, whether or not the incidence of significant suppression or facilitation is constant across SOA. For this, we combined the plots of the time course of SOA-dependent significant modulation, such as Fig. 3F, for suppression and facilitation separately for 260 experimental conditions in which the response to both S1–S2 sequence and S2 alone were tested (Fig. 8). Here again, it can be seen that for collinear S1 conditions, the incidence of significant suppression (Fig. 8B) was much more frequent than that of significant facilitation (Fig. 8A). This difference is not apparent for parallel S1 conditions (compare Fig. 8E and F). The time course of modulation was also different; for collinear S1 conditions, suppressive modulation was concentrated at around 100 ms after S2 onset (Fig. 8C), which corresponded to the time of peak response to S2 alone, whereas facilitative modulation was relatively more dispersed (Fig. 8E). For parallel S1 conditions, facilitation was dominant after about 200 ms following S2 onset.

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