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The development of cortical circuits for motion discrimination.

Smith GB, Sederberg A, Elyada YM, Van Hooser SD, Kaschube M, Fitzpatrick D - Nat. Neurosci. (2015)

Bottom Line: Over the next three weeks, the population response becomes increasingly sparse, wave-like activity disappears, and variability and noise correlations are markedly reduced.Furthermore, experience with a moving stimulus was capable of driving a reduction in noise correlations over a matter of hours.These changes in variability and correlation contribute significantly to a marked improvement in direction discriminability over development.

View Article: PubMed Central - PubMed

Affiliation: Department of Functional Architecture and Development of Cerebral Cortex, Max Planck Florida Institute for Neuroscience, Jupiter, Florida, USA.

ABSTRACT
Stimulus discrimination depends on the selectivity and variability of neural responses, as well as the size and correlation structure of the responsive population. For direction discrimination in visual cortex, only the selectivity of neurons has been well characterized across development. Here we show in ferrets that at eye opening, the cortical response to visual stimulation exhibits several immaturities, including a high density of active neurons that display prominent wave-like activity, a high degree of variability and strong noise correlations. Over the next three weeks, the population response becomes increasingly sparse, wave-like activity disappears, and variability and noise correlations are markedly reduced. Similar changes were observed in identified neuronal populations imaged repeatedly over days. Furthermore, experience with a moving stimulus was capable of driving a reduction in noise correlations over a matter of hours. These changes in variability and correlation contribute significantly to a marked improvement in direction discriminability over development.

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Correlation between decrease in noise correlation and direction selectivity(a) Pairwise noise correlations decrease significantly from the initial to the final imaging session. Red dot indicates mean across all pairs and animals. (b) Relationship between change in pairwise noise correlation and direction selectivity (relative to day 0) for 4 animals in which chronic imaging was performed. In 3 of 4 cases, noise correlations exhibited a significant decrease by the final imaging session, whereas direction selectivity significantly increased (n = 33, 147, and 126 neurons per experiment). In one experiment (F1319, shown in orange, n=13 neurons) neither changes in DSI nor correlations were significant. Data are shown as mean ± SEM across all neurons. Averaging across all neurons and pairs on the final imaging session (black line) reveals a significant decrease in noise correlation and a significant rise in direction selectivity. (c) Cartoon depicting possible relationships in pairwise angular preference across imaging sessions. (d) Initial pairwise noise correlations are higher for pairs that will maintain similar preferences (S-S pairs) than those that adopt opposite preferences (S-O pairs). (e) Initial correlations are higher for pairs with opposite preferences if that pair will adopt matching preferred directions on the final imaging session (O-S) than for pairs that maintain opposite preferences (O-O).
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Figure 6: Correlation between decrease in noise correlation and direction selectivity(a) Pairwise noise correlations decrease significantly from the initial to the final imaging session. Red dot indicates mean across all pairs and animals. (b) Relationship between change in pairwise noise correlation and direction selectivity (relative to day 0) for 4 animals in which chronic imaging was performed. In 3 of 4 cases, noise correlations exhibited a significant decrease by the final imaging session, whereas direction selectivity significantly increased (n = 33, 147, and 126 neurons per experiment). In one experiment (F1319, shown in orange, n=13 neurons) neither changes in DSI nor correlations were significant. Data are shown as mean ± SEM across all neurons. Averaging across all neurons and pairs on the final imaging session (black line) reveals a significant decrease in noise correlation and a significant rise in direction selectivity. (c) Cartoon depicting possible relationships in pairwise angular preference across imaging sessions. (d) Initial pairwise noise correlations are higher for pairs that will maintain similar preferences (S-S pairs) than those that adopt opposite preferences (S-O pairs). (e) Initial correlations are higher for pairs with opposite preferences if that pair will adopt matching preferred directions on the final imaging session (O-S) than for pairs that maintain opposite preferences (O-O).

Mentions: These changes in single-cell response were accompanied by a significant decline in pairwise noise correlation amongst the longitudinally imaged populations (Fig. 6a, Supplementary Fig. 3, WSR: Z(18946)=–98.10, p<0.001, n=18948 pairs). We next assessed the relationship between the change in selectivity of individual neurons and the structure of the population response during the period following eye opening (Fig. 6b). In 3 of 4 longitudinal imaging experiments, direction selectivity had increased from the initial to the final imaging session (Friedman’s test: p<0.05 for each experiment with 33, 147, and 126 neurons per experiment, respectively, statistics in Supplementary table 3), while pairwise noise correlations amongst this same population decreased (Friedman’s test: p<0.001 for each experiment, with 489, 10618, and 7770 pairs per experiment, respectively, statistics in Supplementary table 3). In the fourth experiment, only 13 neurons were both identifiable and visually responsive across days and neither changes in in direction selectivity nor in noise correlation were significant (Friedman’s test: direction selectivity: p=0.58, n=13 cells, correlation: p=0.49, n=69 pairs). We also observed a strong decrease in trial-to trial variability over this same period (initial vs. final imaging session, WSR: Z(317)=15.48, p<0.001). These results clearly show that individual neurons in defined populations become both more selective for direction of motion, less variable, and less correlated following eye opening.


The development of cortical circuits for motion discrimination.

Smith GB, Sederberg A, Elyada YM, Van Hooser SD, Kaschube M, Fitzpatrick D - Nat. Neurosci. (2015)

Correlation between decrease in noise correlation and direction selectivity(a) Pairwise noise correlations decrease significantly from the initial to the final imaging session. Red dot indicates mean across all pairs and animals. (b) Relationship between change in pairwise noise correlation and direction selectivity (relative to day 0) for 4 animals in which chronic imaging was performed. In 3 of 4 cases, noise correlations exhibited a significant decrease by the final imaging session, whereas direction selectivity significantly increased (n = 33, 147, and 126 neurons per experiment). In one experiment (F1319, shown in orange, n=13 neurons) neither changes in DSI nor correlations were significant. Data are shown as mean ± SEM across all neurons. Averaging across all neurons and pairs on the final imaging session (black line) reveals a significant decrease in noise correlation and a significant rise in direction selectivity. (c) Cartoon depicting possible relationships in pairwise angular preference across imaging sessions. (d) Initial pairwise noise correlations are higher for pairs that will maintain similar preferences (S-S pairs) than those that adopt opposite preferences (S-O pairs). (e) Initial correlations are higher for pairs with opposite preferences if that pair will adopt matching preferred directions on the final imaging session (O-S) than for pairs that maintain opposite preferences (O-O).
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Related In: Results  -  Collection

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Figure 6: Correlation between decrease in noise correlation and direction selectivity(a) Pairwise noise correlations decrease significantly from the initial to the final imaging session. Red dot indicates mean across all pairs and animals. (b) Relationship between change in pairwise noise correlation and direction selectivity (relative to day 0) for 4 animals in which chronic imaging was performed. In 3 of 4 cases, noise correlations exhibited a significant decrease by the final imaging session, whereas direction selectivity significantly increased (n = 33, 147, and 126 neurons per experiment). In one experiment (F1319, shown in orange, n=13 neurons) neither changes in DSI nor correlations were significant. Data are shown as mean ± SEM across all neurons. Averaging across all neurons and pairs on the final imaging session (black line) reveals a significant decrease in noise correlation and a significant rise in direction selectivity. (c) Cartoon depicting possible relationships in pairwise angular preference across imaging sessions. (d) Initial pairwise noise correlations are higher for pairs that will maintain similar preferences (S-S pairs) than those that adopt opposite preferences (S-O pairs). (e) Initial correlations are higher for pairs with opposite preferences if that pair will adopt matching preferred directions on the final imaging session (O-S) than for pairs that maintain opposite preferences (O-O).
Mentions: These changes in single-cell response were accompanied by a significant decline in pairwise noise correlation amongst the longitudinally imaged populations (Fig. 6a, Supplementary Fig. 3, WSR: Z(18946)=–98.10, p<0.001, n=18948 pairs). We next assessed the relationship between the change in selectivity of individual neurons and the structure of the population response during the period following eye opening (Fig. 6b). In 3 of 4 longitudinal imaging experiments, direction selectivity had increased from the initial to the final imaging session (Friedman’s test: p<0.05 for each experiment with 33, 147, and 126 neurons per experiment, respectively, statistics in Supplementary table 3), while pairwise noise correlations amongst this same population decreased (Friedman’s test: p<0.001 for each experiment, with 489, 10618, and 7770 pairs per experiment, respectively, statistics in Supplementary table 3). In the fourth experiment, only 13 neurons were both identifiable and visually responsive across days and neither changes in in direction selectivity nor in noise correlation were significant (Friedman’s test: direction selectivity: p=0.58, n=13 cells, correlation: p=0.49, n=69 pairs). We also observed a strong decrease in trial-to trial variability over this same period (initial vs. final imaging session, WSR: Z(317)=15.48, p<0.001). These results clearly show that individual neurons in defined populations become both more selective for direction of motion, less variable, and less correlated following eye opening.

Bottom Line: Over the next three weeks, the population response becomes increasingly sparse, wave-like activity disappears, and variability and noise correlations are markedly reduced.Furthermore, experience with a moving stimulus was capable of driving a reduction in noise correlations over a matter of hours.These changes in variability and correlation contribute significantly to a marked improvement in direction discriminability over development.

View Article: PubMed Central - PubMed

Affiliation: Department of Functional Architecture and Development of Cerebral Cortex, Max Planck Florida Institute for Neuroscience, Jupiter, Florida, USA.

ABSTRACT
Stimulus discrimination depends on the selectivity and variability of neural responses, as well as the size and correlation structure of the responsive population. For direction discrimination in visual cortex, only the selectivity of neurons has been well characterized across development. Here we show in ferrets that at eye opening, the cortical response to visual stimulation exhibits several immaturities, including a high density of active neurons that display prominent wave-like activity, a high degree of variability and strong noise correlations. Over the next three weeks, the population response becomes increasingly sparse, wave-like activity disappears, and variability and noise correlations are markedly reduced. Similar changes were observed in identified neuronal populations imaged repeatedly over days. Furthermore, experience with a moving stimulus was capable of driving a reduction in noise correlations over a matter of hours. These changes in variability and correlation contribute significantly to a marked improvement in direction discriminability over development.

Show MeSH
Related in: MedlinePlus