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Augusto A Lempel

Kristina J Nielsen

(2021)
Development of visual motion integration involves coordination of multiple cortical stages

eLife 10:e59798.

https://doi.org/10.7554/eLife.59798
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Additional files

8 figures, 2 tables and 1 additional file

Figures

Figure 1 with 1 supplement

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Pattern and component cells are found in PSS across all ages tested.

(A) Sagittal view of the ferret brain indicating the location of PSS and V1 (ss: suprasylvian sulcus). (B) Top: Plaid stimuli with different angles between the component directions (dOri). Bottom: …

Figure 1—figure supplement 1

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PSS direction selectivity is mature at P37.

(A) Direction tuning curves of example PSS neurons at P37 (left) and in an adult animal (right), as measured with gratings. The DSI is indicated for each neuron (see Materials and methods). Error …

Figure 2 with 1 supplement

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Motion integration in PSS matures around P41.

(A) Median PSS pattern index for each animal included in the study, plotted as a function of age. Gray dots represent animals that yielded one to two neurons, black dots represent animals with data …

Figure 2—source data 1 Neuron-by-neuron metrics for Figure 2 and Figure 2—figure supplement 1.: https://cdn.elifesciences.org/articles/59798/elife-59798-fig2-data1-v2.xlsx
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Changes in pattern and component correlation contribute to the developmental increase in pattern index.

Cumulative distributions of pattern (left) and component (right) correlations for PSS cells recorded in different age groups. Data recorded using the streaming stimulus paradigm. For statistical …

Figure 3

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Longer visual experience results in a higher degree of PSS motion integration.

(A) Median PSS pattern index for each animal aged P37–40, plotted as a function of visual experience. Gray dots represent animals that yielded 1–2 neurons, and black dots represent animals with data …

Figure 3—source data 1 Neuron-by-neuron metrics for Figure 3.: https://cdn.elifesciences.org/articles/59798/elife-59798-fig3-data1-v2.xlsx
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Figure 4 with 1 supplement

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Responses of PSS neurons to plaid stimuli become increasingly modulated by dOri with development, especially in pattern cells.

(A) Average 2D profile of PSS responses to plaids at different ages (plotted in same format as Figure 1D–E). Average response profiles were computed by normalizing the data for each neuron by its …

Figure 4—source data 1 Neuron-by-neuron metrics for Figure 4 and Figure 5—figure supplement 1.: https://cdn.elifesciences.org/articles/59798/elife-59798-fig4-data1-v2.xlsx
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Relative plaid responses in PSS and the Wilson–Hilferty transformation.

(A) Average relative plaid response in PSS as a function of dOri. For each age group, curves indicate the median (solid line) and upper and lower 25th percentile (dotted lines). (B) Distribution of …

Figure 5 with 1 supplement

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V1 responses to plaids change during PSS motion integration development.

(A) Average 2D profile of responses to plaids in V1 at different ages (computed and plotted as in Figure 4A). (B) Average relative plaid response in V1 as a function of dOri (data shown after …

Figure 5—source data 1 Neuron-by-neuron metrics for Figure 5 and Figure 5—figure supplement 1.: https://cdn.elifesciences.org/articles/59798/elife-59798-fig5-data1-v2.xlsx
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Motion integration levels in V1 are lower than those in PSS across development.

Cumulative distribution of pattern indices for cells recorded in V1 (solid line) and PSS (dashed line) at different ages. Left: P37–40. Middle: P44–47. Right: Adults.

***p<0.001.

Figure 6

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Changes in V1 responses at P44–47 depend on feedback from PSS.

(A) Average relative plaid response in V1 at P37–40 (same data as Figure 5B), P44–47 (same data as Figure 5B), and P44–47 with muscimol inactivation of PSS. Error bars indicate ± SEM. Data are shown …

Figure 6—source data 1 Neuron-by-neuron metrics for Figure 6.: https://cdn.elifesciences.org/articles/59798/elife-59798-fig6-data1-v2.xlsx
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A computational model of the ferret motion pathway for testing mechanisms behind motion integration development.

(A) Diagram of the model used to explain PSS plaid responses across development. The first stage was composed of 16 V1 direction selective cells whose responses were modeled after empirical V1 data …

Figure 7—source data 1 Neuron-by-neuron metrics for Figure 7.: https://cdn.elifesciences.org/articles/59798/elife-59798-fig7-data1-v2.xlsx
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Figure 8 with 1 supplement

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Effects of changes in V1 and PSS mechanisms on PSS plaid responses.

Summary of different instantiations of the motion pathway model. (A) Baseline model. (B) Model with increased PSS inhibition. (C) Model with increased PSS excitation . (D) Model with V1 responses …

Figure 8—source data 1 Neuron-by-neuron metrics for Figure 8 and Figure 8—figure supplement 1.: https://cdn.elifesciences.org/articles/59798/elife-59798-fig8-data1-v2.xlsx
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Figure 8—figure supplement 1

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Changes in PSS inhibition parameters with development and model parameter settings for the different model instantiations.

(A) Changes in the two model variables that control PSS inhibition (K_I, left; I, right) with development, determined by fitting the model to data from the two age groups, with the V1 stage set to …

Tables

Table 1

Extended information for all statistical analyses.

Figure	Experimental groups	Metric or variable	Test	p-value	Other stats
Figure 1 Sup 1	P37 vs adult	Direction selectivity index	Welch’s t-test	0.86	d’ = 0.04

Figure 2A	P37–40 vs P41–47	Animal median pattern index	Welch’s t-test	0.002	d’ = 1.1
Figure 2A	P37–40 vs adult	Animal median pattern index	Welch’s t-test	0.001	d’ = 1.4
Figure 2A	P41–47 vs adult	Animal median pattern index	Welch’s t-test	0.59	d’ = 0.23
Figure 2A	P37–40 vs P41–47	Animal median pattern index	Resample test	<0.001
Figure 2A	P37–40 vs adult	Animal median pattern index	Resample test	<0.001

Figure 2B	P37–40 vs P41–47	Pattern index. Multiple dOri	Welch’s t-test	<0.001	d’ = 0.74
Figure 2B	P37–40 vs adult	Pattern index. Multiple dOri	Welch’s t-test	<0.001	d’ = 0.96
Figure 2B	P41–47 vs adult	Pattern index. Multiple dOri	Welch’s t-test	0.3	d’ = 0.19
Figure 2B	P37–40 vs P41–47	Pattern index. Multiple dOri	Resample test	<0.001
Figure 2B	P37–40 vs adult	Pattern index. Multiple dOri	Resample test	<0.001

Figure 2 Sup 1	P37–40 vs P41–47	Z_p. Multiple dOri	Welch’s t-test	<0.001	d’ = 0.74
Figure 2 Sup 1	P37–40 vs adult	Z_p. Multiple dOri	Welch’s t-test	<0.001	d’ = 1.0
Figure 2 Sup 1	P41–47 vs adult	Z_p. Multiple dOri	Welch’s t-test	0.24	d’ = 0.22
Figure 2 Sup 1	P37–40 vs P41–47	Z_p. Multiple dOri	Resample test	<0.001
Figure 2 Sup 1	P37–40 vs adult	Z_p. Multiple dOri	Resample test	<0.001

Figure 2 Sup 1	P37–40 vs P41–47	Z_c. Multiple dOri	Welch’s t-test	<0.001	d’ = 0.61
Figure 2 Sup 1	P37–40 vs adult	Z_c. Multiple dOri	Welch’s t-test	<0.001	d’ = 0.73
Figure 2 Sup 1	P41–47 vs adult	Z_c. Multiple dOri	Welch’s t-test	0.58	d’ = 0.10
Figure 2 Sup 1	P37–40 vs P41–47	Z_c. Multiple dOri	Resample test	<0.001
Figure 2 Sup 1	P37–40 vs adult	Z_c. Multiple dOri	Resample test	<0.001

Figure 2E	P37–40 vs P41–47	Pattern index. dOri 135 deg	Welch’s t-test	<0.001	d’ = 1.3
Figure 2E	P37–40 vs adult	Pattern index. dOri 135 deg	Welch’s t-test	<0.001	d’ = 0.94
Figure 2E	P41–47 vs adult	Pattern index. dOri 135 deg	Welch’s t-test	0.43	d’ = 0.21
Figure 2E	P37–40 vs P41–47	Pattern index. dOri 135 deg	Resample test	<0.001
Figure 2E	P37–40 vs adult	Pattern index. dOri 135 deg	Resample test	0.005

Figure 3A	V4 vs V5	Median pattern index	Welch’s t-test	0.005	d’ = 1.8
Figure 3A	V4 vs V6	Median pattern index	Welch’s t-test	0.02	d’ = 1.3
Figure 3A	V5 vs V6	Median pattern index	Welch’s t-test	0.89	d’ = 0.07
Figure 3C	V4 vs V5–6	Pattern index	Welch’s t-test	0.01	d’ = 0.5
Figure 3C	V4 vs V5–6	Pattern index	Resample test	0.03
Figure 3D	V4 vs V5–6	Z_p	Welch’s t-test	0.03	d’ = 0.42
Figure 3D	V4 vs V5–6	Z_p	Resample test	0.04
Figure 3D	V4 vs V5–6	Z_c	Welch’s t-test	0.02	d’ = 0.52
Figure 3D	V4 vs V5–6	Z_c	Resample test	0.03

Figure 4B	P37–40 vs P41–47	Relative plaid responses. Wilson–Hilferty transform	ANOVA. Var: age.	0.80	F = 0.07
Figure 4B	P37–40 vs P41–47	Relative plaid responses. Wilson–Hilferty transform.	ANOVA. Var: dOri	<0.001	F = 60
Figure 4B	P37–40 vs P41–47	Relative plaid responses. Wilson–Hilferty transform.	ANOVA. Var: interaction	0.006	F = 3
Figure 4B	P37–40 vs adult	Relative plaid responses. Wilson–Hilferty transform.	ANOVA. Var: age.	0.08	F = 3.1
Figure 4B	P37–40 vs adult	Relative plaid responses. Wilson–Hilferty transform.	ANOVA. Var: dOri	<0.001	F = 44
Figure 4B	P37–40 vs adult	Relative plaid responses. Wilson–Hilferty transform.	ANOVA. Var: interaction	<0.001	F = 4.2
Figure 4B	P41–47 vs adult	Relative plaid responses. Wilson–Hilferty transform.	ANOVA. Var: age.	0.16	F = 2
Figure 4B	P41–47 vs adult	Relative plaid responses. Wilson–Hilferty transform.	ANOVA. Var: dOri	<0.001	F = 51
Figure 4B	P41–47 vs adult	Relative plaid responses. Wilson–Hilferty transform.	ANOVA. Var: interaction	0.64	F = 0.7

Figure 4B	P37–40 vs P41–47	Relative plaid responses. dOri: 45 deg. Wilson–Hilferty transform.	Welch’s t-test	0.16	d’=0.19
Figure 4B	P37–40 vs adult	Relative plaid responses. dOri: 45 deg. Wilson–Hilferty transform.	Welch’s t-test	0.005	d’ = 0.58
Figure 4B	P41–47 vs adult	Relative plaid responses. dOri: 45 deg. Wilson-Hilferty transform.	Welch’s t-test	0.06	d’ = 0.39
Figure 4B	P37–40 vs adult	Relative plaid responses. dOri: 45 deg. Wilson–Hilferty transform.	Resample test	<0.001

Figure 4B	P37–40 vs P41–47	Relative plaid responses. dOri: 157 deg. Wilson–Hilferty transform.	Welch’s t-test	0.02	0.32
Figure 4B	P37–40 vs adult	Relative plaid responses. dOri: 157 deg. Wilson–Hilferty transform.	Welch’s t-test	0.01	0.42
Figure 4B	P41–47 vs adult	Relative plaid responses. dOri: 157 deg. Wilson–Hilferty transform.	Welch’s t-test	0.53	0.12
Figure 4B	P37–40 vs P41–47	Relative plaid responses. dOri: 157 deg. Wilson–Hilferty transform.	Resample test	0.002
Figure 4B	P37–40 vs adult	Relative plaid responses. dOri: 157 deg. Wilson–Hilferty transform.	Resample test	<0.001

Figure 4C	P37–40	Pattern index vs relative plaid response. Wilson–Hilferty transform	Pearson correlation	0.009	r = 0.21
Figure 4C	P41–47	Pattern index vs relative plaid response. Wilson–Hilferty transform.	Pearson correlation	<0.001	r = 0.46
Figure 4C	Adult	Pattern index vs relative plaid response. Wilson–Hilferty transform	Pearson correlation	<0.001	r = 0.60
Figure 4C	P47–40 vs adult	Pattern index vs relative plaid response. Wilson–Hilferty transform	Correlation difference	0.02	z = 2.06
Figure 4C	P47–40 vs P41–47	Pattern index vs relative plaid response. Wilson–Hilferty transform	Correlation difference	0.003	z = 2.77

Figure 4 Sup 1C	P37–40	Pattern index vs relative plaid response.	Pearson correlation	0.003	r = 0.24
Figure 4 Sup 1C	P41–47	Pattern index vs relative plaid response.	Pearson correlation	<0.001	r = 0.46
Figure 4 Sup 1C	Adult	Pattern index vs relative plaid response.	Pearson correlation	<0.001	r = 0.58

Figure 5B	P37–40 vs P44–47	Relative plaid responses. Wilson–Hilferty transform	ANOVA. Var: age.	0.001	F = 11
Figure 5B	P37–40 vs P44–47	Relative plaid responses. Wilson–Hilferty transform.	ANOVA. Var: dOri	<0.001	F = 11
Figure 5B	P37–40 vs P44–47	Relative plaid responses. Wilson–Hilferty transform.	ANOVA. Var: interaction	0.26	F = 1.3
Figure 5B	P37–40 vs adult	Relative plaid responses. Wilson–Hilferty transform.	ANOVA. Var: age.	<0.001	F = 82
Figure 5B	P37–40 vs adult	Relative plaid responses. Wilson–Hilferty transform.	ANOVA. Var: dOri	<0.001	F = 6.8
Figure 5B	P37–40 vs adult	Relative plaid responses. Wilson-Hilferty transform.	ANOVA. Var: interaction	0.10	F = 1.8
Figure 5B	P44–47 vs adult	Relative plaid responses. Wilson–Hilferty transform.	ANOVA. Var: age	<0.001	F = 100
Figure 5B	P44–47 vs adult	Relative plaid responses. Wilson–Hilferty transform.	ANOVA. Var: dOri	<0.001	F = 7
Figure 5B	P44–47 vs adult	Relative plaid responses. Wilson–Hilferty transform.	ANOVA. Var: interaction	0.03	F = 2.3

Figure 5D	P37–40 vs P44–47	Pattern index. dOri 135 deg	Welch’s t-test	<0.001	d’ = 0.61
Figure 5D	P37–40 vs adult	Pattern index. dOri 135 deg	Welch’s t-test	0.94	d’ = 0.01
Figure 5D	P44–47 vs adult	Pattern index. dOri 135 deg	Welch’s t-test	<0.001	d’ = 0.64
Figure 5D	P44–47 vs adult	Pattern index. dOri 135 deg	Resample test	<0.001

Figure 6A	P44–47 vs muscimol	Relative plaid responses. Wilson–Hilferty transform	ANOVA. Var: Muscimol.	<0.001	F = 17
Figure 6A	P44–47 vs muscimol	Relative plaid responses. Wilson–Hilferty transform.	ANOVA. Var: dOri	<0.001	F = 4.5
Figure 6A	P44–47 vs muscimol	Relative plaid responses. Wilson–Hilferty transform.	ANOVA. Var: interaction	0.44	F = 0.97
Figure 6C	P44-47 vs ACSF	Relative plaid responses. Wilson–Hilferty transform.	ANOVA. Var: ACSF.	0.56	F = 0.32
Figure 6C	P44–47 vs ACSF	Relative plaid responses. Wilson–Hilferty transform.	ANOVA. Var: dOri	<0.001	F = 8.3
Figure 6C	P44–47 vs ACSF	Relative plaid responses. Wilson–Hilferty transform.	ANOVA. Var: interaction	0.98	F = 0.20
Figure 6A	P37–40 vs muscimol	Relative plaid responses. Wilson–Hilferty transform	ANOVA. Var: Muscimol.	0.04	F = 4.3
Figure 6A	P37–40 vs muscimol	Relative plaid responses. Wilson–Hilferty transform.	ANOVA. Var: dOri	0.007	F = 3.0
Figure 6A	P37–40 vs muscimol	Relative plaid responses. Wilson–Hilferty transform.	ANOVA. Var: interaction	0.94	F = 0.29
Figure 6C	P37–40 vs ACSF	Relative plaid responses. Wilson–Hilferty transform.	ANOVA. Var: ACSF.	<0.001	F = 12
Figure 6C	P37–40 vs ACSF	Relative plaid responses. Wilson–Hilferty transform.	ANOVA. Var: dOri	<0.001	F = 6.6
Figure 6C	P37–40 vs ACSF	Relative plaid responses. Wilson–Hilferty transform.	ANOVA. Var: interaction	0.42	F = 1

Figure 6B	P44–47 vs muscimol	Pattern index	Welch’s t-test	0.01	d’ = 0.52
Figure 6D	P44–47 vs ACSF	Pattern index	Welch’s t-test	0.4	d’ = 0.15
Figure 6B	P37–41 vs muscimol	Pattern index	Welch’s t-test	0.71	d’ = 0.07
Figure 6D	P37–41 vs ACSF	Pattern index	Welch’s t-test	0.02	d’ = 0.46
Figure 6B	P44–47 vs muscimol	Pattern index	Resample test	0.02
Figure 6B	P37–41 vs ACSF	Pattern index	Resample test	0.01

Figure 7C	P37–40 vs P44–47	Model-data correlation	Rank-sum test	0.14
Figure 7E	P37–40 vs P44–47	Model excitation (W_exc)	Rank-sum test	0.06
Figure 7E	P37–40 vs P44–47	Model inhibition (W_inh)	Rank-sum test	<0.001
Figure 7E	P37–40 vs P44–47	Model PSS threshold (T_PSS)	Rank-sum test	0.96
Figure 7E	P37–40 vs P44–47	Model inhibition (W_inh)	Resample test	<0.001

Table 2

Number of animals and neurons for all experiments.

Figures	Experiment/analysis	Experimental group	Animals	Neurons
1 Sup 1	Analysis of direction selectivity using gratings.	PSS. P37.	3	37
1 Sup 1	Analysis of direction selectivity using gratings.	PSS. Adult.	10	68
1, 2, and 4	Analysis of pattern index and dOri tuning using responses to plaids of different dOri values.	PSS. P37–40.	27	153
1, 2, and 4	Analysis of pattern index and dOri tuning using responses to plaids of different dOri values.	PSS. P41–47.	13	84
1, 2, and 4	Analysis of pattern index and dOri tuning using responses to plaids of different dOri values.	PSS. Adult.	9	46
3	Analysis of pattern index and dOri tuning using responses to plaids of different dOri values.	PSS. V4.	4	33
3	Analysis of pattern index and dOri tuning using responses to plaids of different dOri values.	PSS. V5.	8	34
3	Analysis of pattern index and dOri tuning using responses to plaids of different dOri values.	PSS. P37.	6	36
3	Analysis of pattern index and dOri tuning using responses to plaids of different dOri values.	PSS. P40.	8	38
2 Sup 1	Analysis of pattern index using responses to plaids of dOri 135 deg.	PSS. P37–40.	6	12
2 Sup 1	Analysis of pattern index using responses to plaids of dOri 135 deg.	PSS. P41–47.	5	23
2 Sup 1	Analysis of pattern index using responses to plaids of dOri 135 deg.	PSS. Adult.	7	35
5, 6	Analysis of pattern index and dOri tuning using responses to plaids of different dOri values.	V1. P37–40.	16	97
5, 6	Analysis of pattern index and dOri tuning using responses to plaids of different dOri values.	V1. P41-47.	14	115
5	Analysis of pattern index and dOri tuning using responses to plaids of different dOri values.	V1. Adult.	9	40
6	Analysis of pattern index and dOri tuning using responses to plaids of different dOri values.	Muscimol	5	38
6	Analysis of pattern index and dOri tuning using responses to plaids of different dOri values.	ACSF	3	38
7, 8	Analysis of model MLE fits.	PSS. P37-40.	25	136
7	Analysis of model MLE fits.	PSS. P44-47.	8	46