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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.


Population analysis of the orientation selectivity and preference                                of the lateral synaptic input explored by intracellular                                recordings. (A) The orientation tuning for each                            cluster of activation observed in the subthreshold receptive field of                            eight analyzed cells was computed (18 clusters, open squares). The                            preferred orientation (relative to the cell's preferred                            orientation at spiking level) is plotted as a function of the circular                            variance (tuning strength). (B) We computed the expected                            optical signal from the responses obtained for each orientation                            condition in each cluster, realigned with each cell's preferred                            orientation. Each data point corresponds to the normalized level of                            activity obtained in each cluster for the tested orientations. Gray                            curve: the resulting fitted population orientation tuning.
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Figure 10: Population analysis of the orientation selectivity and preference of the lateral synaptic input explored by intracellular recordings. (A) The orientation tuning for each cluster of activation observed in the subthreshold receptive field of eight analyzed cells was computed (18 clusters, open squares). The preferred orientation (relative to the cell's preferred orientation at spiking level) is plotted as a function of the circular variance (tuning strength). (B) We computed the expected optical signal from the responses obtained for each orientation condition in each cluster, realigned with each cell's preferred orientation. Each data point corresponds to the normalized level of activity obtained in each cluster for the tested orientations. Gray curve: the resulting fitted population orientation tuning.

Mentions: These experiments were conducted in the Department of Integrative and Computational Neuroscience (UNIC) at CNRS (Gif-sur-Yvette, France). Long-duration (>1 h) intracellular recordings were performed in the area centralis representation (Horsley–Clarke coordinates P: 1.5–2.5, L: 1.5) in cat area 17. RF dynamics were studied both at the spiking and at the subthreshold level in 25 cells. Eight cells (out of 14) were selected for the Gabor dense noise analysis (Figure 7) and 11 cells were used to compare the orientation tuning of peripheral vs. center responses (Figure 10).


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)

Population analysis of the orientation selectivity and preference                                of the lateral synaptic input explored by intracellular                                recordings. (A) The orientation tuning for each                            cluster of activation observed in the subthreshold receptive field of                            eight analyzed cells was computed (18 clusters, open squares). The                            preferred orientation (relative to the cell's preferred                            orientation at spiking level) is plotted as a function of the circular                            variance (tuning strength). (B) We computed the expected                            optical signal from the responses obtained for each orientation                            condition in each cluster, realigned with each cell's preferred                            orientation. Each data point corresponds to the normalized level of                            activity obtained in each cluster for the tested orientations. Gray                            curve: the resulting fitted population orientation tuning.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 10: Population analysis of the orientation selectivity and preference of the lateral synaptic input explored by intracellular recordings. (A) The orientation tuning for each cluster of activation observed in the subthreshold receptive field of eight analyzed cells was computed (18 clusters, open squares). The preferred orientation (relative to the cell's preferred orientation at spiking level) is plotted as a function of the circular variance (tuning strength). (B) We computed the expected optical signal from the responses obtained for each orientation condition in each cluster, realigned with each cell's preferred orientation. Each data point corresponds to the normalized level of activity obtained in each cluster for the tested orientations. Gray curve: the resulting fitted population orientation tuning.
Mentions: These experiments were conducted in the Department of Integrative and Computational Neuroscience (UNIC) at CNRS (Gif-sur-Yvette, France). Long-duration (>1 h) intracellular recordings were performed in the area centralis representation (Horsley–Clarke coordinates P: 1.5–2.5, L: 1.5) in cat area 17. RF dynamics were studied both at the spiking and at the subthreshold level in 25 cells. Eight cells (out of 14) were selected for the Gabor dense noise analysis (Figure 7) and 11 cells were used to compare the orientation tuning of peripheral vs. center responses (Figure 10).

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.