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A precise form of divisive suppression supports population coding in the primary visual cortex.

MacEvoy SP, Tucker TR, Fitzpatrick D - Nat. Neurosci. (2009)

Bottom Line: The responses of neurons in the primary visual cortex (V1) to an optimally oriented grating are suppressed when a non-optimal grating is superimposed.Using intrinsic signal optical imaging, we found that patterns of tree shrew V1 activity evoked by superimposed equal-contrast gratings were predicted by the averages of patterns evoked by individual component gratings.This prediction held across contrasts, for summed sinusoidal gratings or nonsumming square-wave gratings, and was evident in single-unit extracellular recordings.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurobiology, Duke University Medical Center, Durham, North Carolina, USA. macevoy@psych.upenn.edu

ABSTRACT
The responses of neurons in the primary visual cortex (V1) to an optimally oriented grating are suppressed when a non-optimal grating is superimposed. Although cross-orientation suppression is thought to reflect mechanisms that maintain a distributed code for orientation, the effect of superimposed gratings on V1 population responses is unknown. Using intrinsic signal optical imaging, we found that patterns of tree shrew V1 activity evoked by superimposed equal-contrast gratings were predicted by the averages of patterns evoked by individual component gratings. This prediction held across contrasts, for summed sinusoidal gratings or nonsumming square-wave gratings, and was evident in single-unit extracellular recordings. Intracellular recordings revealed consistent levels of suppression throughout the time course of subthreshold responses. These results indicate that divisive suppression powerfully governs population responses to multiple orientations. Moreover, the specific form of suppression that we observed appears to support independent population codes for stimulus orientation and strength and calls for a reassessment of mechanisms that underlie cross-orientation suppression.

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Responses to superimposed sinusoidal gratings at different contrasts. (a,c) PRPs from one animal evoked by drifting sinusoidal gratings at 45° and 135° presented singly and as summed pairs, color coded as in Fig. 2. Contrasts of both gratings were 25% in a and 12.5% in c. Data in c were scaled according to maximum and minimum values in a. (b,d) Combined PRP data from three animals for contrast of 25% and 12.5%, respectively. (e,f) Single-animal PRPs for dissimilar component contrasts.
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Figure 3: Responses to superimposed sinusoidal gratings at different contrasts. (a,c) PRPs from one animal evoked by drifting sinusoidal gratings at 45° and 135° presented singly and as summed pairs, color coded as in Fig. 2. Contrasts of both gratings were 25% in a and 12.5% in c. Data in c were scaled according to maximum and minimum values in a. (b,d) Combined PRP data from three animals for contrast of 25% and 12.5%, respectively. (e,f) Single-animal PRPs for dissimilar component contrasts.

Mentions: These results indicate that divisive suppression tightly controls population responses to non-summing superimposed gratings. This result appears to be inconsistent with recent models suggesting that cross-orientation suppression results from LGN saturation occurring only under conditions generated by drifting summed sinusoidal gratings26, 27. However, it is possible that the suppression we observed with stationary non-additive gratings was different from suppression that results from summed superimposed gratings. To address this possibility, we repeated our experiment in three animals using drifting sinusoidal gratings. As with non-summing gratings, PRPs for summed sinusoids were well predicted by the mean of their component PRPs (Fig. 3a,b). The ability of the component mean to accurately predict responses to multiple orientations for both additive and non-additive stimuli suggests that cross-orientation suppression is not limited to a particular stimulus configuration, but reflects a more generalized mechanism that regulates overall levels of population activity induced by stimuli that contain multiple orientations.


A precise form of divisive suppression supports population coding in the primary visual cortex.

MacEvoy SP, Tucker TR, Fitzpatrick D - Nat. Neurosci. (2009)

Responses to superimposed sinusoidal gratings at different contrasts. (a,c) PRPs from one animal evoked by drifting sinusoidal gratings at 45° and 135° presented singly and as summed pairs, color coded as in Fig. 2. Contrasts of both gratings were 25% in a and 12.5% in c. Data in c were scaled according to maximum and minimum values in a. (b,d) Combined PRP data from three animals for contrast of 25% and 12.5%, respectively. (e,f) Single-animal PRPs for dissimilar component contrasts.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2875123&req=5

Figure 3: Responses to superimposed sinusoidal gratings at different contrasts. (a,c) PRPs from one animal evoked by drifting sinusoidal gratings at 45° and 135° presented singly and as summed pairs, color coded as in Fig. 2. Contrasts of both gratings were 25% in a and 12.5% in c. Data in c were scaled according to maximum and minimum values in a. (b,d) Combined PRP data from three animals for contrast of 25% and 12.5%, respectively. (e,f) Single-animal PRPs for dissimilar component contrasts.
Mentions: These results indicate that divisive suppression tightly controls population responses to non-summing superimposed gratings. This result appears to be inconsistent with recent models suggesting that cross-orientation suppression results from LGN saturation occurring only under conditions generated by drifting summed sinusoidal gratings26, 27. However, it is possible that the suppression we observed with stationary non-additive gratings was different from suppression that results from summed superimposed gratings. To address this possibility, we repeated our experiment in three animals using drifting sinusoidal gratings. As with non-summing gratings, PRPs for summed sinusoids were well predicted by the mean of their component PRPs (Fig. 3a,b). The ability of the component mean to accurately predict responses to multiple orientations for both additive and non-additive stimuli suggests that cross-orientation suppression is not limited to a particular stimulus configuration, but reflects a more generalized mechanism that regulates overall levels of population activity induced by stimuli that contain multiple orientations.

Bottom Line: The responses of neurons in the primary visual cortex (V1) to an optimally oriented grating are suppressed when a non-optimal grating is superimposed.Using intrinsic signal optical imaging, we found that patterns of tree shrew V1 activity evoked by superimposed equal-contrast gratings were predicted by the averages of patterns evoked by individual component gratings.This prediction held across contrasts, for summed sinusoidal gratings or nonsumming square-wave gratings, and was evident in single-unit extracellular recordings.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurobiology, Duke University Medical Center, Durham, North Carolina, USA. macevoy@psych.upenn.edu

ABSTRACT
The responses of neurons in the primary visual cortex (V1) to an optimally oriented grating are suppressed when a non-optimal grating is superimposed. Although cross-orientation suppression is thought to reflect mechanisms that maintain a distributed code for orientation, the effect of superimposed gratings on V1 population responses is unknown. Using intrinsic signal optical imaging, we found that patterns of tree shrew V1 activity evoked by superimposed equal-contrast gratings were predicted by the averages of patterns evoked by individual component gratings. This prediction held across contrasts, for summed sinusoidal gratings or nonsumming square-wave gratings, and was evident in single-unit extracellular recordings. Intracellular recordings revealed consistent levels of suppression throughout the time course of subthreshold responses. These results indicate that divisive suppression powerfully governs population responses to multiple orientations. Moreover, the specific form of suppression that we observed appears to support independent population codes for stimulus orientation and strength and calls for a reassessment of mechanisms that underlie cross-orientation suppression.

Show MeSH
Related in: MedlinePlus