Limits...
Lateral Spread of Orientation Selectivity in V1 is Controlled by Intracortical Cooperativity.

Chavane F, Sharon D, Jancke D, Marre O, Frégnac Y, Grinvald A - Front Syst Neurosci (2011)

Bottom Line: To understand the role of these lateral interactions, it is crucial to characterize their effective functional connectivity and tuning properties.In contrast, when the stimulus size was increased, we observed orientation-selective spread of activation beyond the feedforward imprint.We conclude that stimulus-induced cooperativity enhances the long-range orientation-selective spread.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurobiology, Weizmann Institute of Science Rehovot, Israel.

ABSTRACT
Neurons in the primary visual cortex receive subliminal information originating from the periphery of their receptive fields (RF) through a variety of cortical connections. In the cat primary visual cortex, long-range horizontal axons have been reported to preferentially bind to distant columns of similar orientation preferences, whereas feedback connections from higher visual areas provide a more diverse functional input. To understand the role of these lateral interactions, it is crucial to characterize their effective functional connectivity and tuning properties. However, the overall functional impact of cortical lateral connections, whatever their anatomical origin, is unknown since it has never been directly characterized. Using direct measurements of postsynaptic integration in cat areas 17 and 18, we performed multi-scale assessments of the functional impact of visually driven lateral networks. Voltage-sensitive dye imaging showed that local oriented stimuli evoke an orientation-selective activity that remains confined to the cortical feedforward imprint of the stimulus. Beyond a distance of one hypercolumn, the lateral spread of cortical activity gradually lost its orientation preference approximated as an exponential with a space constant of about 1 mm. Intracellular recordings showed that this loss of orientation selectivity arises from the diversity of converging synaptic input patterns originating from outside the classical RF. In contrast, when the stimulus size was increased, we observed orientation-selective spread of activation beyond the feedforward imprint. We conclude that stimulus-induced cooperativity enhances the long-range orientation-selective spread.

No MeSH data available.


Orientation selectivity vanishes along the lateral spread, in                                response to a local oriented stimulus. Examples are from area                            17 (A–C, same as Figure 1) and area 18 (D–F).                                (A,D) Time-series of polar orientation maps. The white                            contour delineates the region within which pixels are significantly                            selective to orientation (see Appendix). Time after stimulus onset is given above each                            frame. (B,E) Polar map averaged over the latest time frames                            of the response (indicated above the frame). Contours delineate the                            outer border of the cortical domain within which significant activation                            level (thin gray contour, see Figure 1A) or significant orientation-selective response (thick                            white contour) are observed. (C,F) Spatial extent of the                            activated area (gray) and of its orientation-selective component (black)                            as a function of time. Red line indicates the expected limit of the                            feedforward imprint, as computed in Figure 1. Dotted red line indicates the retinotopic area of the                            stimulus representation. Inset: The spatial extent of the activation                            spread (gray) and the orientation-selective activation (black) are shown                            in comparison with the expected limit of the feedforward imprint                            (red).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3100672&req=5

Figure 3: Orientation selectivity vanishes along the lateral spread, in response to a local oriented stimulus. Examples are from area 17 (A–C, same as Figure 1) and area 18 (D–F). (A,D) Time-series of polar orientation maps. The white contour delineates the region within which pixels are significantly selective to orientation (see Appendix). Time after stimulus onset is given above each frame. (B,E) Polar map averaged over the latest time frames of the response (indicated above the frame). Contours delineate the outer border of the cortical domain within which significant activation level (thin gray contour, see Figure 1A) or significant orientation-selective response (thick white contour) are observed. (C,F) Spatial extent of the activated area (gray) and of its orientation-selective component (black) as a function of time. Red line indicates the expected limit of the feedforward imprint, as computed in Figure 1. Dotted red line indicates the retinotopic area of the stimulus representation. Inset: The spatial extent of the activation spread (gray) and the orientation-selective activation (black) are shown in comparison with the expected limit of the feedforward imprint (red).

Mentions: Figure 3 shows the orientation tuning of the spread for two examples in area 17 (Figures 3A–C) and area 18 (Figures 3D–F). In marked contrast to the pattern of widely spreading activation that expanded continuously during the response time-course (white contour in Figure 1A), the significant orientation-selective component remained spatially confined throughout the whole time-course of the response (white contour in Figures 3A,D; also compare white and gray contours in Figures 3B,E, corresponding respectively to the averaged orientation-selective and activated areas; see Movie S1 in Supplementary Material). This result is in agreement with the prediction of the second hypothesis (Figure 2B), which postulates that the lateral spread activates columns independently of their preferred orientation. In these examples, the largest orientation-selective cortical area was found to be restricted to an average value of 5.5 mm2 (area 17) and 4.2 mm2 (area 18), comparable to the areas of the predicted feedforward imprints (see inset of Figures 3C,F, and compare the black and red contours corresponding respectively to the orientation-selective area and the predicted feedforward imprint limit), whereas an area of 31.3 mm2 and 29.1 mm2 (ER: 3.2 and 3.1 mm) was significantly activated for the same hemispheres. Note that, for the area 18 example, the retinotopic representation of the horizontal visual axis is elongated along the antero-posterior cortical axis, as expected for this area (Tusa et al., 1979). These results were consistent across cortices (n = 9, Figure 4A): the orientation-selective area averaged over nine hemispheres was 5.5 ± 1.4 mm2 (ER: 1.3 ± 0.2 mm), while the global activation gradually recruited the whole imaged cortex equivalent to 26.2 ± 2.7 mm2. Note that these areas are much larger than the number of pixels that are spontaneously active above significance level (see spurious activation at frame 0 ms in Figure 1A and 3A,D, and baseline level in Figures 3C,F).


Lateral Spread of Orientation Selectivity in V1 is Controlled by Intracortical Cooperativity.

Chavane F, Sharon D, Jancke D, Marre O, Frégnac Y, Grinvald A - Front Syst Neurosci (2011)

Orientation selectivity vanishes along the lateral spread, in                                response to a local oriented stimulus. Examples are from area                            17 (A–C, same as Figure 1) and area 18 (D–F).                                (A,D) Time-series of polar orientation maps. The white                            contour delineates the region within which pixels are significantly                            selective to orientation (see Appendix). Time after stimulus onset is given above each                            frame. (B,E) Polar map averaged over the latest time frames                            of the response (indicated above the frame). Contours delineate the                            outer border of the cortical domain within which significant activation                            level (thin gray contour, see Figure 1A) or significant orientation-selective response (thick                            white contour) are observed. (C,F) Spatial extent of the                            activated area (gray) and of its orientation-selective component (black)                            as a function of time. Red line indicates the expected limit of the                            feedforward imprint, as computed in Figure 1. Dotted red line indicates the retinotopic area of the                            stimulus representation. Inset: The spatial extent of the activation                            spread (gray) and the orientation-selective activation (black) are shown                            in comparison with the expected limit of the feedforward imprint                            (red).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3100672&req=5

Figure 3: Orientation selectivity vanishes along the lateral spread, in response to a local oriented stimulus. Examples are from area 17 (A–C, same as Figure 1) and area 18 (D–F). (A,D) Time-series of polar orientation maps. The white contour delineates the region within which pixels are significantly selective to orientation (see Appendix). Time after stimulus onset is given above each frame. (B,E) Polar map averaged over the latest time frames of the response (indicated above the frame). Contours delineate the outer border of the cortical domain within which significant activation level (thin gray contour, see Figure 1A) or significant orientation-selective response (thick white contour) are observed. (C,F) Spatial extent of the activated area (gray) and of its orientation-selective component (black) as a function of time. Red line indicates the expected limit of the feedforward imprint, as computed in Figure 1. Dotted red line indicates the retinotopic area of the stimulus representation. Inset: The spatial extent of the activation spread (gray) and the orientation-selective activation (black) are shown in comparison with the expected limit of the feedforward imprint (red).
Mentions: Figure 3 shows the orientation tuning of the spread for two examples in area 17 (Figures 3A–C) and area 18 (Figures 3D–F). In marked contrast to the pattern of widely spreading activation that expanded continuously during the response time-course (white contour in Figure 1A), the significant orientation-selective component remained spatially confined throughout the whole time-course of the response (white contour in Figures 3A,D; also compare white and gray contours in Figures 3B,E, corresponding respectively to the averaged orientation-selective and activated areas; see Movie S1 in Supplementary Material). This result is in agreement with the prediction of the second hypothesis (Figure 2B), which postulates that the lateral spread activates columns independently of their preferred orientation. In these examples, the largest orientation-selective cortical area was found to be restricted to an average value of 5.5 mm2 (area 17) and 4.2 mm2 (area 18), comparable to the areas of the predicted feedforward imprints (see inset of Figures 3C,F, and compare the black and red contours corresponding respectively to the orientation-selective area and the predicted feedforward imprint limit), whereas an area of 31.3 mm2 and 29.1 mm2 (ER: 3.2 and 3.1 mm) was significantly activated for the same hemispheres. Note that, for the area 18 example, the retinotopic representation of the horizontal visual axis is elongated along the antero-posterior cortical axis, as expected for this area (Tusa et al., 1979). These results were consistent across cortices (n = 9, Figure 4A): the orientation-selective area averaged over nine hemispheres was 5.5 ± 1.4 mm2 (ER: 1.3 ± 0.2 mm), while the global activation gradually recruited the whole imaged cortex equivalent to 26.2 ± 2.7 mm2. Note that these areas are much larger than the number of pixels that are spontaneously active above significance level (see spurious activation at frame 0 ms in Figure 1A and 3A,D, and baseline level in Figures 3C,F).

Bottom Line: To understand the role of these lateral interactions, it is crucial to characterize their effective functional connectivity and tuning properties.In contrast, when the stimulus size was increased, we observed orientation-selective spread of activation beyond the feedforward imprint.We conclude that stimulus-induced cooperativity enhances the long-range orientation-selective spread.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurobiology, Weizmann Institute of Science Rehovot, Israel.

ABSTRACT
Neurons in the primary visual cortex receive subliminal information originating from the periphery of their receptive fields (RF) through a variety of cortical connections. In the cat primary visual cortex, long-range horizontal axons have been reported to preferentially bind to distant columns of similar orientation preferences, whereas feedback connections from higher visual areas provide a more diverse functional input. To understand the role of these lateral interactions, it is crucial to characterize their effective functional connectivity and tuning properties. However, the overall functional impact of cortical lateral connections, whatever their anatomical origin, is unknown since it has never been directly characterized. Using direct measurements of postsynaptic integration in cat areas 17 and 18, we performed multi-scale assessments of the functional impact of visually driven lateral networks. Voltage-sensitive dye imaging showed that local oriented stimuli evoke an orientation-selective activity that remains confined to the cortical feedforward imprint of the stimulus. Beyond a distance of one hypercolumn, the lateral spread of cortical activity gradually lost its orientation preference approximated as an exponential with a space constant of about 1 mm. Intracellular recordings showed that this loss of orientation selectivity arises from the diversity of converging synaptic input patterns originating from outside the classical RF. In contrast, when the stimulus size was increased, we observed orientation-selective spread of activation beyond the feedforward imprint. We conclude that stimulus-induced cooperativity enhances the long-range orientation-selective spread.

No MeSH data available.