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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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Modulation window.The cell of Fig. 3 is reproduced. (A) Response to S2 alone with the duration of 63 ms for inital transient response indicated with red dotted lines. (B) The duration of suppression by S1 at the position c is indicated with two green dotted lines. (C, D) Modulation window formed by the two durations in A and B in corresponding colors. Time of S1 onset is shown in a white line, interpolated across SOA. The S2-alone condition is given above for comparison in C. Note that the range of significant suppression and facilitation agrees well with modulation window. Also note that modulation is variable depending on SOA within modulation window.
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pone-0047543-g004: Modulation window.The cell of Fig. 3 is reproduced. (A) Response to S2 alone with the duration of 63 ms for inital transient response indicated with red dotted lines. (B) The duration of suppression by S1 at the position c is indicated with two green dotted lines. (C, D) Modulation window formed by the two durations in A and B in corresponding colors. Time of S1 onset is shown in a white line, interpolated across SOA. The S2-alone condition is given above for comparison in C. Note that the range of significant suppression and facilitation agrees well with modulation window. Also note that modulation is variable depending on SOA within modulation window.

Mentions: The fact that SOAs were not equally effective in modulating spike response was likely related to the neural latency of S1, i.e., the time it took from presentation of S1 to the start of modulation manifested at the neuron under study. Since S1 alone did not evoke a response, and the suppressive or facilitative modulation was only manifested in the neural response to S2, the modulation occurred only within a time window determined by both the duration of the spike response to S2 and the duration of the S1 effect. Typically, it was difficult to estimate the time course of modulatory effects of S1, but in rare cases, the response to S1 alone caused a suppression of spike activity. This point is illustrated in Fig. 4, reproducing the response of the cell of Fig. 3. The S1 at the position c did not excite the cell, but suppressed the spontaneous activity later (Fig. 4B), allowing estimation of suppression duration. Suppression and facilitation in response to the S1–S2 sequence can be partly explained by the sum of the time course of excitatory response to S2 alone (Fig. 4A) and the time course of response to S1 alone (Fig. 4B). The combined time course constitutes a window of response modulation (Fig. 4C). The temporal window for suppressive and facilitative modulation corresponded fairly well to the combined time course (Fig. 4C, D). For example, the decrease in spontaneous activity (green dotted lines) and ensuing increase in Fig. 4B are reflected in the temporal range of significant suppression and facilitation in Fig. 4D. We emphasize, however, that within this window, modulation was not constant, but varied depending on SOA. In other words, response to the S1–S2 sequence was not completely explained by a (weighted) sum of SOA-adjusted individual responses to S1 and S2 alone. For example, in Fig. 4D, within the windows of suppressive and facilitative modulation defined by the combined time courses, the suppression was significant at an SOA of 50 ms, but not for SOA of 40 or 60 ms.


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

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

Modulation window.The cell of Fig. 3 is reproduced. (A) Response to S2 alone with the duration of 63 ms for inital transient response indicated with red dotted lines. (B) The duration of suppression by S1 at the position c is indicated with two green dotted lines. (C, D) Modulation window formed by the two durations in A and B in corresponding colors. Time of S1 onset is shown in a white line, interpolated across SOA. The S2-alone condition is given above for comparison in C. Note that the range of significant suppression and facilitation agrees well with modulation window. Also note that modulation is variable depending on SOA within modulation window.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3472985&req=5

pone-0047543-g004: Modulation window.The cell of Fig. 3 is reproduced. (A) Response to S2 alone with the duration of 63 ms for inital transient response indicated with red dotted lines. (B) The duration of suppression by S1 at the position c is indicated with two green dotted lines. (C, D) Modulation window formed by the two durations in A and B in corresponding colors. Time of S1 onset is shown in a white line, interpolated across SOA. The S2-alone condition is given above for comparison in C. Note that the range of significant suppression and facilitation agrees well with modulation window. Also note that modulation is variable depending on SOA within modulation window.
Mentions: The fact that SOAs were not equally effective in modulating spike response was likely related to the neural latency of S1, i.e., the time it took from presentation of S1 to the start of modulation manifested at the neuron under study. Since S1 alone did not evoke a response, and the suppressive or facilitative modulation was only manifested in the neural response to S2, the modulation occurred only within a time window determined by both the duration of the spike response to S2 and the duration of the S1 effect. Typically, it was difficult to estimate the time course of modulatory effects of S1, but in rare cases, the response to S1 alone caused a suppression of spike activity. This point is illustrated in Fig. 4, reproducing the response of the cell of Fig. 3. The S1 at the position c did not excite the cell, but suppressed the spontaneous activity later (Fig. 4B), allowing estimation of suppression duration. Suppression and facilitation in response to the S1–S2 sequence can be partly explained by the sum of the time course of excitatory response to S2 alone (Fig. 4A) and the time course of response to S1 alone (Fig. 4B). The combined time course constitutes a window of response modulation (Fig. 4C). The temporal window for suppressive and facilitative modulation corresponded fairly well to the combined time course (Fig. 4C, D). For example, the decrease in spontaneous activity (green dotted lines) and ensuing increase in Fig. 4B are reflected in the temporal range of significant suppression and facilitation in Fig. 4D. We emphasize, however, that within this window, modulation was not constant, but varied depending on SOA. In other words, response to the S1–S2 sequence was not completely explained by a (weighted) sum of SOA-adjusted individual responses to S1 and S2 alone. For example, in Fig. 4D, within the windows of suppressive and facilitative modulation defined by the combined time courses, the suppression was significant at an SOA of 50 ms, but not for SOA of 40 or 60 ms.

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