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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.


Statistical significance of orientation tuning of                                            intracellular responses evoked by peripheral local                                            stimulation. Difference between activities evoked                                        by local stimuli of orthogonal orientations was tested using                                        a two-tailed t-test. (A,B)                                        present the examples of two different clusters of activity                                        taken from the two cells presented in Figure 9 [A: Figure                                            9D (triangle);                                            B: Figure 9F (square)]. The time-course of the activation                                        for orthogonal orientations are presented in a color code                                        (cyan and red for horizontal and vertical; green and purple                                        for obliques), below which the dynamic of the                                            t-value is presented in black (limit of                                        1 and 5% significance is shown). In (A), the                                        horizontal orientation (red) evokes a significantly higher                                        response than vertical orientation (cyan), whereas the                                        reverse is observed in (B). Same conventions as                                        in Figure 7C.                                        Population analysis: for each cluster of activity we applied                                        the same t-test, and the maximum of the                                            t-value observed for the two couple of                                        orthogonal orientations is displayed as a function of the                                        relative preferred orientation of the activity evoked by                                        that cluster (compared to the cell's preferred                                        orientation). No particular bias in orientation preference                                        (established on the subpopulation of orientation-selective                                        clusters) was observed.
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FA3: Statistical significance of orientation tuning of intracellular responses evoked by peripheral local stimulation. Difference between activities evoked by local stimuli of orthogonal orientations was tested using a two-tailed t-test. (A,B) present the examples of two different clusters of activity taken from the two cells presented in Figure 9 [A: Figure 9D (triangle); B: Figure 9F (square)]. The time-course of the activation for orthogonal orientations are presented in a color code (cyan and red for horizontal and vertical; green and purple for obliques), below which the dynamic of the t-value is presented in black (limit of 1 and 5% significance is shown). In (A), the horizontal orientation (red) evokes a significantly higher response than vertical orientation (cyan), whereas the reverse is observed in (B). Same conventions as in Figure 7C. Population analysis: for each cluster of activity we applied the same t-test, and the maximum of the t-value observed for the two couple of orthogonal orientations is displayed as a function of the relative preferred orientation of the activity evoked by that cluster (compared to the cell's preferred orientation). No particular bias in orientation preference (established on the subpopulation of orientation-selective clusters) was observed.

Mentions: The first cell (Figures 9C,D) illustrates a case of lateral recruitment by a diversity of oriented inputs. Peripheral “hot spots” significantly activate the recorded neuron after a delay compatible with horizontal propagation at slow speed (Bringuier et al., 1999). These peripheral positions also evoke subthreshold significant orientation-selective responses but with an orientation preference depending on their location (square and triangle in Figure 9D, see another example with late peripheral responses, Movie S2 in Supplementary Material). The second cell (Figures 9E,F) illustrates a case of an untuned peripheral response. The peripheral hot spot indicated by a triangle (Figure 9F) shows significant response strength but no orientation selectivity. See Figure A3 in Appendix for a detailed quantification of the orientation-tuned responses and their statistical significance. Note that at short-range distances (square) the observed iso-orientation bias is similar to that observed with VSDI (see another example as Movie S3 in Supplementary Material).


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)

Statistical significance of orientation tuning of                                            intracellular responses evoked by peripheral local                                            stimulation. Difference between activities evoked                                        by local stimuli of orthogonal orientations was tested using                                        a two-tailed t-test. (A,B)                                        present the examples of two different clusters of activity                                        taken from the two cells presented in Figure 9 [A: Figure                                            9D (triangle);                                            B: Figure 9F (square)]. The time-course of the activation                                        for orthogonal orientations are presented in a color code                                        (cyan and red for horizontal and vertical; green and purple                                        for obliques), below which the dynamic of the                                            t-value is presented in black (limit of                                        1 and 5% significance is shown). In (A), the                                        horizontal orientation (red) evokes a significantly higher                                        response than vertical orientation (cyan), whereas the                                        reverse is observed in (B). Same conventions as                                        in Figure 7C.                                        Population analysis: for each cluster of activity we applied                                        the same t-test, and the maximum of the                                            t-value observed for the two couple of                                        orthogonal orientations is displayed as a function of the                                        relative preferred orientation of the activity evoked by                                        that cluster (compared to the cell's preferred                                        orientation). No particular bias in orientation preference                                        (established on the subpopulation of orientation-selective                                        clusters) was observed.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

FA3: Statistical significance of orientation tuning of intracellular responses evoked by peripheral local stimulation. Difference between activities evoked by local stimuli of orthogonal orientations was tested using a two-tailed t-test. (A,B) present the examples of two different clusters of activity taken from the two cells presented in Figure 9 [A: Figure 9D (triangle); B: Figure 9F (square)]. The time-course of the activation for orthogonal orientations are presented in a color code (cyan and red for horizontal and vertical; green and purple for obliques), below which the dynamic of the t-value is presented in black (limit of 1 and 5% significance is shown). In (A), the horizontal orientation (red) evokes a significantly higher response than vertical orientation (cyan), whereas the reverse is observed in (B). Same conventions as in Figure 7C. Population analysis: for each cluster of activity we applied the same t-test, and the maximum of the t-value observed for the two couple of orthogonal orientations is displayed as a function of the relative preferred orientation of the activity evoked by that cluster (compared to the cell's preferred orientation). No particular bias in orientation preference (established on the subpopulation of orientation-selective clusters) was observed.
Mentions: The first cell (Figures 9C,D) illustrates a case of lateral recruitment by a diversity of oriented inputs. Peripheral “hot spots” significantly activate the recorded neuron after a delay compatible with horizontal propagation at slow speed (Bringuier et al., 1999). These peripheral positions also evoke subthreshold significant orientation-selective responses but with an orientation preference depending on their location (square and triangle in Figure 9D, see another example with late peripheral responses, Movie S2 in Supplementary Material). The second cell (Figures 9E,F) illustrates a case of an untuned peripheral response. The peripheral hot spot indicated by a triangle (Figure 9F) shows significant response strength but no orientation selectivity. See Figure A3 in Appendix for a detailed quantification of the orientation-tuned responses and their statistical significance. Note that at short-range distances (square) the observed iso-orientation bias is similar to that observed with VSDI (see another example as Movie S3 in Supplementary Material).

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.