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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.


Propagation of iso-orientation preference emerges from spatial                                summation (visualized by VSDI). (A) Time-series                            of polar representation of orientation maps in area 18 in response to                            full-field (top), local (middle 3° diameter at 5.6°                            eccentricity), and annular stimuli (bottom, inner diameter 6°,                            outer diameter 9°) whose position relative to the local stimulus                            is shown in the stimulus cartoon on the left. White contours delineate                            the cortical regions significantly selective to orientation. Time from                            stimulus onset is indicated above each frame. Bottom right:                            single-condition maps of responses evoked by two adjacent stimuli.                            Ellipses indicate the estimated cortical limit of the stimulus's                            retinotopic representation (see Figure 1). Bottom-right inset: stimuli locations in the visual                            space. Scale bars are 1 mm. (B) Dynamics of the                            cortical areas significantly activated (gray) or orientation selective                            (black) in response to the full-field, local disk, and annular stimuli                            were compared within a cortical region receiving a comparable                            feedforward drive. This region was defined as an elongated region of                            interest (ROI) aligned on the representation axis of the upper-to-lower                            stimuli (reddish rectangle). (C) Another example from area                            18 is shown. Stimulus size was 4° diameter for the local                            stimulus (6°, 7° eccentricity), 8° for the inner                            diameter of the annulus, outer diameter 12°.
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Figure 11: Propagation of iso-orientation preference emerges from spatial summation (visualized by VSDI). (A) Time-series of polar representation of orientation maps in area 18 in response to full-field (top), local (middle 3° diameter at 5.6° eccentricity), and annular stimuli (bottom, inner diameter 6°, outer diameter 9°) whose position relative to the local stimulus is shown in the stimulus cartoon on the left. White contours delineate the cortical regions significantly selective to orientation. Time from stimulus onset is indicated above each frame. Bottom right: single-condition maps of responses evoked by two adjacent stimuli. Ellipses indicate the estimated cortical limit of the stimulus's retinotopic representation (see Figure 1). Bottom-right inset: stimuli locations in the visual space. Scale bars are 1 mm. (B) Dynamics of the cortical areas significantly activated (gray) or orientation selective (black) in response to the full-field, local disk, and annular stimuli were compared within a cortical region receiving a comparable feedforward drive. This region was defined as an elongated region of interest (ROI) aligned on the representation axis of the upper-to-lower stimuli (reddish rectangle). (C) Another example from area 18 is shown. Stimulus size was 4° diameter for the local stimulus (6°, 7° eccentricity), 8° for the inner diameter of the annulus, outer diameter 12°.

Mentions: Two different VSDI examples are presented in Figure 11. In the first example (Figure 11A), we compared the polar map dynamics of VSDI responses to a full-field (top row), a local (middle row, 3° diameter) and an annular grating (bottom row, inner diameter of 6°, outer diameter 9°) precisely encroaching on the outer border of the local stimulus (see drawing on the left). As reported above, the orientation-selective component activated by the local grating remained spatially restricted (middle row, white contour). However, the annular stimulus evoked an orientation-selective response filling in the retinotopic representation of its unstimulated inner disk, which is a region devoid of direct feedforward input (bottom row). The inner ring retinotopic representation can be inferred from the retinotopic maps shown in Figure 11A (right). The lower position (continuous ellipse) corresponds to the retinotopic activation of the lower stimulus: in the middle row it is activated directly by the local patch; in the lower row, it is fed by the ring itself. In this latter case, the contiguous cortical zone activated by the upper position (dotted ellipse) corresponds to the retinotopic representation of the unstimulated inner disk of the annular stimulus. To compare the cortical area over which significant orientation-selective response is observed in the three conditions (cartoons in the left panel), we restricted the quantification inside a specific cortical ROI (Figure 11B). This ROI corresponds to a rectangle centered on the representation of the lower stimulus, and aligned to vertical visual axis representation (antero-posterior cortical axis). Therefore, it allows quantifying VSDI responses over a cortical region receiving a same amount of visual stimulation in the local and annular conditions (reddish rectangle superimposed on stimulus cartoon and averaged polar map). Within such ROI, the dynamics of the cortical area becoming significantly orientation selective (delimited by the white contour) is shown in the right column of Figure 11B. Whereas the cortical regions which are significantly activated (gray curve) in the three conditions are comparable, the spatial extent of the orientation-selective cortical area (black curve) is larger for the annular stimulation (bottom row) than the inner disk (middle row). In Figure 11C we show another example that reproduces the same result: the annular stimulus evokes an activation spread inside the cortical representation of the inner disk of the annulus that is selective to orientation.


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)

Propagation of iso-orientation preference emerges from spatial                                summation (visualized by VSDI). (A) Time-series                            of polar representation of orientation maps in area 18 in response to                            full-field (top), local (middle 3° diameter at 5.6°                            eccentricity), and annular stimuli (bottom, inner diameter 6°,                            outer diameter 9°) whose position relative to the local stimulus                            is shown in the stimulus cartoon on the left. White contours delineate                            the cortical regions significantly selective to orientation. Time from                            stimulus onset is indicated above each frame. Bottom right:                            single-condition maps of responses evoked by two adjacent stimuli.                            Ellipses indicate the estimated cortical limit of the stimulus's                            retinotopic representation (see Figure 1). Bottom-right inset: stimuli locations in the visual                            space. Scale bars are 1 mm. (B) Dynamics of the                            cortical areas significantly activated (gray) or orientation selective                            (black) in response to the full-field, local disk, and annular stimuli                            were compared within a cortical region receiving a comparable                            feedforward drive. This region was defined as an elongated region of                            interest (ROI) aligned on the representation axis of the upper-to-lower                            stimuli (reddish rectangle). (C) Another example from area                            18 is shown. Stimulus size was 4° diameter for the local                            stimulus (6°, 7° eccentricity), 8° for the inner                            diameter of the annulus, outer diameter 12°.
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Figure 11: Propagation of iso-orientation preference emerges from spatial summation (visualized by VSDI). (A) Time-series of polar representation of orientation maps in area 18 in response to full-field (top), local (middle 3° diameter at 5.6° eccentricity), and annular stimuli (bottom, inner diameter 6°, outer diameter 9°) whose position relative to the local stimulus is shown in the stimulus cartoon on the left. White contours delineate the cortical regions significantly selective to orientation. Time from stimulus onset is indicated above each frame. Bottom right: single-condition maps of responses evoked by two adjacent stimuli. Ellipses indicate the estimated cortical limit of the stimulus's retinotopic representation (see Figure 1). Bottom-right inset: stimuli locations in the visual space. Scale bars are 1 mm. (B) Dynamics of the cortical areas significantly activated (gray) or orientation selective (black) in response to the full-field, local disk, and annular stimuli were compared within a cortical region receiving a comparable feedforward drive. This region was defined as an elongated region of interest (ROI) aligned on the representation axis of the upper-to-lower stimuli (reddish rectangle). (C) Another example from area 18 is shown. Stimulus size was 4° diameter for the local stimulus (6°, 7° eccentricity), 8° for the inner diameter of the annulus, outer diameter 12°.
Mentions: Two different VSDI examples are presented in Figure 11. In the first example (Figure 11A), we compared the polar map dynamics of VSDI responses to a full-field (top row), a local (middle row, 3° diameter) and an annular grating (bottom row, inner diameter of 6°, outer diameter 9°) precisely encroaching on the outer border of the local stimulus (see drawing on the left). As reported above, the orientation-selective component activated by the local grating remained spatially restricted (middle row, white contour). However, the annular stimulus evoked an orientation-selective response filling in the retinotopic representation of its unstimulated inner disk, which is a region devoid of direct feedforward input (bottom row). The inner ring retinotopic representation can be inferred from the retinotopic maps shown in Figure 11A (right). The lower position (continuous ellipse) corresponds to the retinotopic activation of the lower stimulus: in the middle row it is activated directly by the local patch; in the lower row, it is fed by the ring itself. In this latter case, the contiguous cortical zone activated by the upper position (dotted ellipse) corresponds to the retinotopic representation of the unstimulated inner disk of the annular stimulus. To compare the cortical area over which significant orientation-selective response is observed in the three conditions (cartoons in the left panel), we restricted the quantification inside a specific cortical ROI (Figure 11B). This ROI corresponds to a rectangle centered on the representation of the lower stimulus, and aligned to vertical visual axis representation (antero-posterior cortical axis). Therefore, it allows quantifying VSDI responses over a cortical region receiving a same amount of visual stimulation in the local and annular conditions (reddish rectangle superimposed on stimulus cartoon and averaged polar map). Within such ROI, the dynamics of the cortical area becoming significantly orientation selective (delimited by the white contour) is shown in the right column of Figure 11B. Whereas the cortical regions which are significantly activated (gray curve) in the three conditions are comparable, the spatial extent of the orientation-selective cortical area (black curve) is larger for the annular stimulation (bottom row) than the inner disk (middle row). In Figure 11C we show another example that reproduces the same result: the annular stimulus evokes an activation spread inside the cortical representation of the inner disk of the annulus that is selective to orientation.

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.