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Intervening inhibition underlies simple-cell receptive field structure in visual cortex.

Liu BH, Li P, Sun YJ, Li YT, Zhang LI, Tao HW - Nat. Neurosci. (2009)

Bottom Line: The segregated receptive-field structures were generated by the integration of excitation and inhibition with a stereotypic 'overlap-but-mismatched' pattern: the peaks of excitatory On/Off subfields were separated and flanked colocalized peaks of inhibitory On/Off subfields.The small mismatch of excitation/inhibition led to an asymmetric inhibitory shaping of On/Off spatial tunings, resulting in a great enhancement of their distinctiveness.Thus, slightly separated On/Off excitation, together with intervening inhibition, can create simple-cell receptive-field structure and the dichotomy of receptive-field structures may arise from a fine-tuning of the spatial arrangement of synaptic inputs.

View Article: PubMed Central - PubMed

Affiliation: Zilkha Neurogenetic Institute, Keck School of Medicine, University of Southern California, Los Angeles, California, USA.

ABSTRACT
Synaptic inputs underlying spike receptive fields are important for understanding mechanisms of neuronal processing. Using whole-cell voltage-clamp recordings from neurons in mouse primary visual cortex, we examined the spatial patterns of their excitatory and inhibitory synaptic inputs evoked by On and Off stimuli. Neurons with either segregated or overlapped On/Off spike subfields had substantial overlaps between all the four synaptic subfields. The segregated receptive-field structures were generated by the integration of excitation and inhibition with a stereotypic 'overlap-but-mismatched' pattern: the peaks of excitatory On/Off subfields were separated and flanked colocalized peaks of inhibitory On/Off subfields. The small mismatch of excitation/inhibition led to an asymmetric inhibitory shaping of On/Off spatial tunings, resulting in a great enhancement of their distinctiveness. Thus, slightly separated On/Off excitation, together with intervening inhibition, can create simple-cell receptive-field structure and the dichotomy of receptive-field structures may arise from a fine-tuning of the spatial arrangement of synaptic inputs.

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Grouping of cells based on the structure of synaptic subfields. (a) The distributions of the normalized distances between the peaks of Vm On/Off subfields, and between the excitatory On/Off subfields (Ex). The two distributions are not different (Mann-Whitney test, p = 0.14). The dash line marks norm. distance = 0.32, which was used to group the cells from V-clamp recordings. (b) The distributions of the OIs of Vm and excitatory subfields. Mann-Whitney test, p = 0.21. The dash line marks OI = 0.71, which separated the cells from V-clamp recordings the same as in a. (c) Synaptic subfields and derived spike subfields of six putative S-RF cells. For each cell, shown from left to right are the synaptic tuning curves in the slice that passes through the peaks of the Eon and Eoff, the four synaptic subfields, the derived spike subfields and the superimposed outlines of fitted spike subfields. Color scale: 337, 404,543, 528 pA for synaptic subfields (in the sequence of Eon, Eoff, Ion, Ioff), 15, 10 Hz for spike On/Off subfields in cell #2; 163, 165, 288, 196 pA, 10, 15 Hz in cell #3; 280, 342, 638, 854 pA, 10, 10 Hz in cell #4; 122, 106, 142, 141 pA, 10, 10 Hz in cell #5; 225, 153, 245, 161 pA, 15, 20 Hz in cell #6; 311, 184, 412, 149 pA, 10, 5 Hz in cell #7. (d) Six putative O-RF cells. Plots are organized in the same way as in c. Color scale: 74, 54, 141, 82 pA, 5, 10 Hz in cell #15; 398, 347, 595, 563 pA, 10, 10 Hz in cell #16; 141, 154, 298, 145 pA, 15, 15 Hz in cell #17; 187, 172, 218, 173 pA, 15, 15 Hz in cell #18; 232, 154, 356, 329 pA, 20, 5 Hz in cell #19; 280, 253, 415, 221 pA, 15, 15 Hz in cell #20. (e) OI of derived spike subfields versus the normalized distance between the peaks of the Eon and Eoff for all recorded neurons (n = 33). The vertical and horizontal dash lines mark Ex norm. distance = 0.32 and spike OI = 0.33 respectively. Left, histogram of spike OI. The schematic drawings depict the extent of overlap between two identical subfields for OI = 0, 0.5 and 1 respectively. Bottom, histogram of Ex norm. distance. (f) OI of derived spike subfields vs. the OI between the Eon and Eoff. The vertical and horizontal dash lines mark Ex OI = 0.71 and spike OI = 0.33 respectively. Bottom, the histogram of Ex OI. (g) The distribution of the subfield size of the derived and recorded spike responses. Solid symbol = mean, error bar = SD. *, p < 0.01, t-test.
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Figure 3: Grouping of cells based on the structure of synaptic subfields. (a) The distributions of the normalized distances between the peaks of Vm On/Off subfields, and between the excitatory On/Off subfields (Ex). The two distributions are not different (Mann-Whitney test, p = 0.14). The dash line marks norm. distance = 0.32, which was used to group the cells from V-clamp recordings. (b) The distributions of the OIs of Vm and excitatory subfields. Mann-Whitney test, p = 0.21. The dash line marks OI = 0.71, which separated the cells from V-clamp recordings the same as in a. (c) Synaptic subfields and derived spike subfields of six putative S-RF cells. For each cell, shown from left to right are the synaptic tuning curves in the slice that passes through the peaks of the Eon and Eoff, the four synaptic subfields, the derived spike subfields and the superimposed outlines of fitted spike subfields. Color scale: 337, 404,543, 528 pA for synaptic subfields (in the sequence of Eon, Eoff, Ion, Ioff), 15, 10 Hz for spike On/Off subfields in cell #2; 163, 165, 288, 196 pA, 10, 15 Hz in cell #3; 280, 342, 638, 854 pA, 10, 10 Hz in cell #4; 122, 106, 142, 141 pA, 10, 10 Hz in cell #5; 225, 153, 245, 161 pA, 15, 20 Hz in cell #6; 311, 184, 412, 149 pA, 10, 5 Hz in cell #7. (d) Six putative O-RF cells. Plots are organized in the same way as in c. Color scale: 74, 54, 141, 82 pA, 5, 10 Hz in cell #15; 398, 347, 595, 563 pA, 10, 10 Hz in cell #16; 141, 154, 298, 145 pA, 15, 15 Hz in cell #17; 187, 172, 218, 173 pA, 15, 15 Hz in cell #18; 232, 154, 356, 329 pA, 20, 5 Hz in cell #19; 280, 253, 415, 221 pA, 15, 15 Hz in cell #20. (e) OI of derived spike subfields versus the normalized distance between the peaks of the Eon and Eoff for all recorded neurons (n = 33). The vertical and horizontal dash lines mark Ex norm. distance = 0.32 and spike OI = 0.33 respectively. Left, histogram of spike OI. The schematic drawings depict the extent of overlap between two identical subfields for OI = 0, 0.5 and 1 respectively. Bottom, histogram of Ex norm. distance. (f) OI of derived spike subfields vs. the OI between the Eon and Eoff. The vertical and horizontal dash lines mark Ex OI = 0.71 and spike OI = 0.33 respectively. Bottom, the histogram of Ex OI. (g) The distribution of the subfield size of the derived and recorded spike responses. Solid symbol = mean, error bar = SD. *, p < 0.01, t-test.

Mentions: Synaptic subfields were obtained for a total of 33 neurons. In all of these neurons, the four synaptic subfields substantially overlapped, but there was a relatively larger variation in the separation between the Eon and Eoff (Supplementary Fig. 5). According to spike response data (Fig. 1c), about half of these cells were potential S-RF cells. To understand how different spatial patterns of synaptic inputs result in different spike RF structures, first we roughly categorized the recorded cells into putative S-RF and O-RF cells. As the spatial relationship between the Eon and Eoff primarily determined that of the subthreshold depolarizing responses (Supplementary Fig. 6), and the latter could predict the S-RF/O-RF structures (Fig. 1h,i), we applied the same separation criteria to the patterns of excitatory inputs in order to categorize cells (i.e. S-RF cells having normalized peak distance < 0.32, or OI < 0.71) (Fig. 3a,b). Interestingly, the grouping was the same based on either the OI or the normalized peak distance (Fig. 3b).


Intervening inhibition underlies simple-cell receptive field structure in visual cortex.

Liu BH, Li P, Sun YJ, Li YT, Zhang LI, Tao HW - Nat. Neurosci. (2009)

Grouping of cells based on the structure of synaptic subfields. (a) The distributions of the normalized distances between the peaks of Vm On/Off subfields, and between the excitatory On/Off subfields (Ex). The two distributions are not different (Mann-Whitney test, p = 0.14). The dash line marks norm. distance = 0.32, which was used to group the cells from V-clamp recordings. (b) The distributions of the OIs of Vm and excitatory subfields. Mann-Whitney test, p = 0.21. The dash line marks OI = 0.71, which separated the cells from V-clamp recordings the same as in a. (c) Synaptic subfields and derived spike subfields of six putative S-RF cells. For each cell, shown from left to right are the synaptic tuning curves in the slice that passes through the peaks of the Eon and Eoff, the four synaptic subfields, the derived spike subfields and the superimposed outlines of fitted spike subfields. Color scale: 337, 404,543, 528 pA for synaptic subfields (in the sequence of Eon, Eoff, Ion, Ioff), 15, 10 Hz for spike On/Off subfields in cell #2; 163, 165, 288, 196 pA, 10, 15 Hz in cell #3; 280, 342, 638, 854 pA, 10, 10 Hz in cell #4; 122, 106, 142, 141 pA, 10, 10 Hz in cell #5; 225, 153, 245, 161 pA, 15, 20 Hz in cell #6; 311, 184, 412, 149 pA, 10, 5 Hz in cell #7. (d) Six putative O-RF cells. Plots are organized in the same way as in c. Color scale: 74, 54, 141, 82 pA, 5, 10 Hz in cell #15; 398, 347, 595, 563 pA, 10, 10 Hz in cell #16; 141, 154, 298, 145 pA, 15, 15 Hz in cell #17; 187, 172, 218, 173 pA, 15, 15 Hz in cell #18; 232, 154, 356, 329 pA, 20, 5 Hz in cell #19; 280, 253, 415, 221 pA, 15, 15 Hz in cell #20. (e) OI of derived spike subfields versus the normalized distance between the peaks of the Eon and Eoff for all recorded neurons (n = 33). The vertical and horizontal dash lines mark Ex norm. distance = 0.32 and spike OI = 0.33 respectively. Left, histogram of spike OI. The schematic drawings depict the extent of overlap between two identical subfields for OI = 0, 0.5 and 1 respectively. Bottom, histogram of Ex norm. distance. (f) OI of derived spike subfields vs. the OI between the Eon and Eoff. The vertical and horizontal dash lines mark Ex OI = 0.71 and spike OI = 0.33 respectively. Bottom, the histogram of Ex OI. (g) The distribution of the subfield size of the derived and recorded spike responses. Solid symbol = mean, error bar = SD. *, p < 0.01, t-test.
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Figure 3: Grouping of cells based on the structure of synaptic subfields. (a) The distributions of the normalized distances between the peaks of Vm On/Off subfields, and between the excitatory On/Off subfields (Ex). The two distributions are not different (Mann-Whitney test, p = 0.14). The dash line marks norm. distance = 0.32, which was used to group the cells from V-clamp recordings. (b) The distributions of the OIs of Vm and excitatory subfields. Mann-Whitney test, p = 0.21. The dash line marks OI = 0.71, which separated the cells from V-clamp recordings the same as in a. (c) Synaptic subfields and derived spike subfields of six putative S-RF cells. For each cell, shown from left to right are the synaptic tuning curves in the slice that passes through the peaks of the Eon and Eoff, the four synaptic subfields, the derived spike subfields and the superimposed outlines of fitted spike subfields. Color scale: 337, 404,543, 528 pA for synaptic subfields (in the sequence of Eon, Eoff, Ion, Ioff), 15, 10 Hz for spike On/Off subfields in cell #2; 163, 165, 288, 196 pA, 10, 15 Hz in cell #3; 280, 342, 638, 854 pA, 10, 10 Hz in cell #4; 122, 106, 142, 141 pA, 10, 10 Hz in cell #5; 225, 153, 245, 161 pA, 15, 20 Hz in cell #6; 311, 184, 412, 149 pA, 10, 5 Hz in cell #7. (d) Six putative O-RF cells. Plots are organized in the same way as in c. Color scale: 74, 54, 141, 82 pA, 5, 10 Hz in cell #15; 398, 347, 595, 563 pA, 10, 10 Hz in cell #16; 141, 154, 298, 145 pA, 15, 15 Hz in cell #17; 187, 172, 218, 173 pA, 15, 15 Hz in cell #18; 232, 154, 356, 329 pA, 20, 5 Hz in cell #19; 280, 253, 415, 221 pA, 15, 15 Hz in cell #20. (e) OI of derived spike subfields versus the normalized distance between the peaks of the Eon and Eoff for all recorded neurons (n = 33). The vertical and horizontal dash lines mark Ex norm. distance = 0.32 and spike OI = 0.33 respectively. Left, histogram of spike OI. The schematic drawings depict the extent of overlap between two identical subfields for OI = 0, 0.5 and 1 respectively. Bottom, histogram of Ex norm. distance. (f) OI of derived spike subfields vs. the OI between the Eon and Eoff. The vertical and horizontal dash lines mark Ex OI = 0.71 and spike OI = 0.33 respectively. Bottom, the histogram of Ex OI. (g) The distribution of the subfield size of the derived and recorded spike responses. Solid symbol = mean, error bar = SD. *, p < 0.01, t-test.
Mentions: Synaptic subfields were obtained for a total of 33 neurons. In all of these neurons, the four synaptic subfields substantially overlapped, but there was a relatively larger variation in the separation between the Eon and Eoff (Supplementary Fig. 5). According to spike response data (Fig. 1c), about half of these cells were potential S-RF cells. To understand how different spatial patterns of synaptic inputs result in different spike RF structures, first we roughly categorized the recorded cells into putative S-RF and O-RF cells. As the spatial relationship between the Eon and Eoff primarily determined that of the subthreshold depolarizing responses (Supplementary Fig. 6), and the latter could predict the S-RF/O-RF structures (Fig. 1h,i), we applied the same separation criteria to the patterns of excitatory inputs in order to categorize cells (i.e. S-RF cells having normalized peak distance < 0.32, or OI < 0.71) (Fig. 3a,b). Interestingly, the grouping was the same based on either the OI or the normalized peak distance (Fig. 3b).

Bottom Line: The segregated receptive-field structures were generated by the integration of excitation and inhibition with a stereotypic 'overlap-but-mismatched' pattern: the peaks of excitatory On/Off subfields were separated and flanked colocalized peaks of inhibitory On/Off subfields.The small mismatch of excitation/inhibition led to an asymmetric inhibitory shaping of On/Off spatial tunings, resulting in a great enhancement of their distinctiveness.Thus, slightly separated On/Off excitation, together with intervening inhibition, can create simple-cell receptive-field structure and the dichotomy of receptive-field structures may arise from a fine-tuning of the spatial arrangement of synaptic inputs.

View Article: PubMed Central - PubMed

Affiliation: Zilkha Neurogenetic Institute, Keck School of Medicine, University of Southern California, Los Angeles, California, USA.

ABSTRACT
Synaptic inputs underlying spike receptive fields are important for understanding mechanisms of neuronal processing. Using whole-cell voltage-clamp recordings from neurons in mouse primary visual cortex, we examined the spatial patterns of their excitatory and inhibitory synaptic inputs evoked by On and Off stimuli. Neurons with either segregated or overlapped On/Off spike subfields had substantial overlaps between all the four synaptic subfields. The segregated receptive-field structures were generated by the integration of excitation and inhibition with a stereotypic 'overlap-but-mismatched' pattern: the peaks of excitatory On/Off subfields were separated and flanked colocalized peaks of inhibitory On/Off subfields. The small mismatch of excitation/inhibition led to an asymmetric inhibitory shaping of On/Off spatial tunings, resulting in a great enhancement of their distinctiveness. Thus, slightly separated On/Off excitation, together with intervening inhibition, can create simple-cell receptive-field structure and the dichotomy of receptive-field structures may arise from a fine-tuning of the spatial arrangement of synaptic inputs.

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