The emergence of visual category representations in infants’ brains

  1. Xiaoqian Yan  Is a corresponding author
  2. Sarah Shi Tung
  3. Bella Fascendini
  4. Yulan Diana Chen
  5. Anthony M Norcia
  6. Kalanit Grill-Spector
  1. Department of Psychology, Stanford University, United States
  2. Wu Tsai Neurosciences Institute, Stanford University, United States
  3. Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, China
  4. Neurosciences Program, Stanford University, United States
17 figures, 5 videos, 10 tables and 1 additional file

Figures

Experimental design and stimuli analysis.

(A) Example segments of presentation sequences in which faces (top panel) and limbs (bottom panel) were the target category. Images spanning 12° containing gray-level images of items from different …

Strong visual responses over occipital cortex at the image-update frequency and its harmonics in all age groups.

Each panel shows mean responses across infants in an age group. (A) 3- to 4-month-olds, n=17; (B) 4- to 6-month-olds, n=14; (C) 6- to 8-month-olds, n=15; (D) 12- to 15-month-olds, n=15. Left panels …

Face responses emerge over occipitotemporal electrodes after 4 months of age.

Each panel shows mean responses at the category frequency and its harmonics across infants in an age group. (A) 3- to 4-month-olds, n=17; (B) 4- to 6-month-olds; n=14; (C) 6- to 8-month-olds, n=15; …

Temporal dynamics of category-selective responses as a function of age.

Category-selective responses to (A) faces, (B) limbs, (C) corridors, (D) characters, and (E) cars over left and right occipitotemporal region of interest (ROI). Data are averaged across electrodes …

Successful decoding of faces from mean spatiotemporal responses starting from 4 months of age.

(A) An illustration of winner-takes-all leave-one-out-cross-validation (LOOCV) classifier from mean spatiotemporal response patterns of each category. Spatiotemporal patterns of response for each …

Individual split-half spatiotemporal pattern analyses reveal category information slowly emerges in the visual cortex after 6 months of age.

(A) Representation similarity matrices (RSMs) generated from odd/even split-halves of the spatiotemporal patterns of responses in individual infants. Spatiotemporal patterns for each category are …

Selective responses to items of a category and distinctiveness in distributed patterns develop at different times during the first year of life.

Blue arrows: presence of significant mean region of interest (ROI) category-selective responses in lateral occipital ROIs, combining results of analyses in the frequency and time domains. Yellow …

Appendix 1—figure 1
Robust visual and categorical responses recorded over occipitotemporal and occipital cortex in 20 adults.

(A) Left panel: spatial distribution of visual response at 4.286 Hz and harmonic. Harmonic frequencies are indicated on the top. Right panel: mean Fourier amplitude spectrum across 14 electrodes in …

Appendix 1—figure 2
Adult control: using the same amount of data as infants reveals strong category-selective responses in adults’ occipitotemporal cortex.

(A) Mean Fourier amplitude spectrum across seven (left OT: 57, 58, 59, 63, 64, 65, 68; right OT: 90, 91, 94, 95, 96, 99) electrodes in bilateral occipitotemporal regions of interest (ROIs). Data are …

Appendix 1—figure 3
Adult control: using the same amount of data as infants reveals distributed category-selective responses in adults’ occipitotemporal cortex.

(A) Left: An illustration of winner-takes-all leave-one-out-cross-validation (LOOCV) classifier using the spatiotemporal response patterns of each category. Spatiotemporal patterns of response for …

Appendix 1—figure 4
Grating acuity as a function of age measured with a swept spatial frequency technique combining electroencephalography (EEG).

(A) Acuity growth functions are similar across studies, with acuity increasing from 5 to 8 cycles per degree (cpd) in 3-month-olds to around 10–16 cpd in 6-month-olds. This figure is adapted from Nor…

Appendix 1—figure 5
Visual responses over occipital cortex at the image-update frequency and its harmonics in five category conditions in all age groups.

Each column shows mean responses across infants in an age group for each condition. (A) 3- to 4-month-olds, n=17; (B) 4- to 6-month-olds, n=14; (C) 6- to 8-month-olds, n=15; (D) 12- to …

Appendix 1—figure 6
Limb responses emerge over occipitotemporal electrodes after 6 months of age.

Each panel shows mean responses at the category frequency (0.857 Hz) and its harmonics across infants in an age group. (A) 3- to 4-month-olds, n=17; (B) 4- to 6-month-olds; n=14; (C) 6- to …

Appendix 1—figure 7
Corridor responses emerge over occipitotemporal electrodes after 6 months of age.

Each panel shows mean responses at the category frequency and its harmonics across infants in an age group. (A) 3- to 4-month-olds, n=17; (B) 4- to 6-month-olds; n=14; (C) 6- to 8-month-olds, n=15; …

Appendix 1—figure 8
Significant character responses found over occipitotemporal electrodes at 12–15 months of age.

Each panel shows mean responses at the category frequency (0.857 Hz) and its harmonics across infants in an age group. (A) 3- to 4-month-olds, n=17; (B) 4- to 6-month-olds; n=14; (C) 6- to …

Appendix 1—figure 9
Significant car responses found over occipitotemporal electrodes at 3–4 months of age.

Each panel shows mean responses at the category frequency and its harmonics across infants in an age group. (A) 3- to 4-month-olds, n=17; (B) 4- to 6-month-olds; n=14; (C) 6- to 8-month-olds, n=15; …

Appendix 1—figure 10
Illustration of the winner-takes-all (WTA) classifier.

In each individual, the time series data is split into odd and even trials. We concatenate the time series data from 23 electrodes in the left occipitotemporal, occipital, and right occipitotemporal …

Videos

Video 1
Movie showing Gaussian low-pass filtered face stimuli shown in the experiment at 5 cycles per degree (cpd).
Video 2
Movie showing Gaussian low-pass filtered limb stimuli shown in the experiment at 5 cycles per degree (cpd).
Video 3
Movie showing Gaussian low-pass filtered corridor stimuli shown in the experiment at 5 cycles per degree (cpd).
Video 4
Movie showing Gaussian low-pass filtered character stimuli shown in the experiment at 5 cycles per degree (cpd).
Video 5
Movie showing Gaussian low-pass filtered car stimuli shown in the experiment at 5 cycles per degree (cpd).

Tables

Table 1
Linear mixed models (LMMs).
VariableLMM formulaResults
Peak latency: latency of the peak waveform in each time window; window 1: 60–90 ms or window 2: 90–160 ms for 3- to 4-month-olds, and 90–110 ms for other age groupsPeak latency ~1 + log10(age in days)×time window + (1|participant)Figure 2G.
Appendix 1—table 4
Peak latency ~1 + log10(age in days) + (1|participant)Figure 2H. Appendix 1—table 5
Category-selective response amplitude:
root mean square (RMS) of category-selective response at category frequency (0.857 Hz) and its first harmonic (1.714 Hz)
Response amplitude ~1 + log10(age in days)×category + (1|participant)
Peak amplitude: peak response in a 400–700 ms time windowPeak amplitude ~1 + log10(age in days)×category + (1|participant)Appendix 1—table 7
Peak amplitude ~1 + log10(age in days) + (1|participant)Figure 4. Appendix 1—table 8
Category distinctiveness of spatiotemporal responses for each of the five categoriesCategory distinctiveness ~log10(age in days)×category + (1|participant)
Category distinctiveness ~log10(age in days) + (1|participant)Figure 6B
Appendix 1—table 1
Demographic information.
3–4 months(N=17)4–6 months(N=14)6–8 months(N=15)12–15 months(N=15)
Age at test (days)84–117127–183194–232369–445
Sex
 Female 7 7 6 4
 Male 10 7 9 11
Race
 White 5 4 6 5
 Black
 Asian 1 1 2
 Mixed races 11 8 6 7
 Unknown 1 1 2 1
Appendix 1—table 2
Average number of valid epochs summed across all five categories for each age group before and after data pre-processing.
3–4 months(N=17)4–6 months(N=14)6–8 months(N=15)12–15 months(N=15)Adults(N=20)
Before pre-processing281 (± 103)270 (± 86)346 (± 111)324 (± 78)600 (± 0)
After pre-processing223 (± 89)219 (± 73)266 (± 91)269 (± 77)560 (± 37)
Ratio (after/before)79%81%77%83%93%
Appendix 1—table 3
Mean (± SD) values of contrast, luminance, and similarity metrics across images within each five stimuli categories.
FacesLimbsCorridorsCharactersCars
Contrast0.469
(2.533e-4)
0.391
(3.91e-4)
0.404
(4.04e-4)
0.2856
(2.856e-4)
0.3269
(3.269e-4)
Luminance0.6733
(0.0007)
0.6729
(0.0011)
0.6732
(0.0011)
0.6732
(0.0008)
0.6733
(0.0009)
Similarity0.9855
(0.0063)
0.9555
(0.0039)
0.9569
(0.0051)
0.9563
(0.0033)
0.9570
(0.0044)
Appendix 1—table 4
Peak latency of visual responses by age and time window (window 1: 60–90 ms; window 2: 90–160 ms for 3- to 4-month-olds, and 90–110 ms for other groups).

Formula: Peak latency ~1 + log10(age) × time window + (1|participant). Significant effects are indicated by asterisks.

ParameterβCIdftp
Intercept–54.61−100.82, –8.41118–2.340.021*
Age39.7719.51, 60.021183.890.00017***
Window141.68112.92, 170.451189.757.69e-17***
Age×window–45.78−58.39, –33.17118–7.196.39e-11**
Appendix 1—table 5
Peak latency of visual responses by age at each of the two time windows.

Formula: Peak latency ~1 + log10(age) + (1|participant). Significant effects are indicated by asterisks.

WindowParameterβCIdftp
Window1Intercept90.1975.66, 104.725912.424.22e-18***
Age–7.44−13.82, –1.0659–2.330.02*
Window2Intercept218.09196.05, 240.135919.809.64e-28***
Age–46.91−56.56, –37.2759–9.737.06e-14***
Appendix 1—table 6
Analysis of peak amplitude of visual responses by age and time window.

Formula: Peak amplitude ~1 + log10(age) × time window + (1|participant). Significant effects are indicated by an asterisk.

ParameterβCIdftp
Intercept–18.69−32.35, –5.03118–2.710.008**
Age3.93–2.05, 9.921181.300.20
Window17.248.66, 25.821183.980.0001***
Age×window–4.90−8.66, –1.14118–2.580.011*
Appendix 1—table 7
Peak amplitude of visual responses by age at each of the two time windows.

Formula: Peak amplitude ~1 + log10(age) + (1|participant). Significant effects are indicated by asterisks.

WindowParameterβCIdftp
Window1Intercept1.69–3.42, 6.79590.660.51
Age0.91–1.33, 3.15590.820.42
Window2Intercept11.164.80, 17.51593.510.0009***
Age–3.59−6.38, –0.8159–2.580.012*
Appendix 1—table 8
Analysis of peak amplitude of waveforms of category responses by age and category.

Separate linear mixed models (LMMs) were done separately for the left occipitotemporal (OT) and right OT regions of interest (ROIs). Formula: Peak amplitude ~1 + log10(age) × category + …

ROI/metricParameterβCIdftp
Left OT/Intercept–1.35–7.36, 4.66301–0.440.66
amplitudeAge2.62–0.02, 5.253011.950.052
Category0.18–1.58, 1.933010.200.84
Age×category–0.20–0.97, 0.57301–0.510.61
Left OT/Intercept730.29477.96, 982.613015.702.9e-8***
latencyAge–97.17–207.76, 13.43301–1.730.08
Category–43.35–119.43, 32.73301–1.120.26
Age×category20.24–13.11, 53.583011.190.23
Right OT/Intercept–7.39−14.44, –0.36301–2.070.04*
amplitudeAge5.532.45, 8.623013.530.0005***
Category2.190.06, 4.33012.020.04*
Age×category–1.09−2.00, –0.14301–2.260.02*
Right OT/Intercept922.47667.95, 11773017.137.38e-12***
latencyAge–173.17−284.73, –61.61301–3.050.002**
Category–64.41–141.15, 12.33301–1.650.10
Age×category28.49–5.15, 62.123011.670.10
Appendix 1—table 9
Analysis of peak amplitude of waveforms of category responses for each category in the right occipitotemporal (OT) region of interest (ROI).

Formula: Peak amplitude ~age + (1|participant). Significant effects are indicated by an asterisk.

CategoryParameterβCIdftp
FacesIntercept–10.43−17.81, –3.0559–2.830.006**
Age7.274.03, 10.51594.503.30e-5***
LimbsIntercept2.10–3.62, 7.83590.740.46
Age–2.90−5.41,–0.3859–2.310.02*
CorridorsIntercept–4.65–11.09, 1.8159–1.440.15
Age0.35–2.47, 3.18590.250.80
CharactersIntercept–2.79–8.06, 2.4959–1.060.3
Age–0.66–2.97, 1.6559–0.570.57
CarsIntercept–4.87–11.46, 1.7359–1.480.15
Age0.78–2.11, 3.67590.540.59

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