Anatomy of human sensory cortices reflects inter-individual variability in time estimation - PubMed (original) (raw)

Anatomy of human sensory cortices reflects inter-individual variability in time estimation

Sharon Gilaie-Dotan et al. Front Integr Neurosci. 2011.

Abstract

The ability to estimate duration is essential to human behavior, yet people vary greatly in their ability to estimate time and the brain structures mediating this inter-individual variability remain poorly understood. Here, we showed that inter-individual variability in duration estimation was highly correlated across visual and auditory modalities but depended on the scale of temporal duration. We further examined whether this inter-individual variability in estimating durations of different supra-second time scales (2 or 12 s) was reflected in variability in human brain anatomy. We found that the gray matter volume in both the right posterior lateral sulcus encompassing primary auditory and secondary somatosensory cortex, plus parahippocampal gyrus strongly predicted an individual's ability to discriminate longer durations of 12 s (but not shorter ones of 2 s) regardless of whether they were presented in auditory or visual modalities. Our findings suggest that these brain areas may play a common role in modality-independent time discrimination. We propose that an individual's ability to discriminate longer durations is linked to self-initiated rhythm maintenance mechanisms relying on the neural structure of these modality-specific sensory and parahippocampal cortices.

Keywords: VBM; individual differences; modality-independent; neural structure; supra-seconds time perception.

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Figures

Figure 1

Figure 1

Experimental design (A) Depiction of a duration discrimination trial, presented either visually or aurally for shorter (2 s) or longer (12 s) durations. Trials were blocked by condition and lasted for target duration (2 or 12 s respectively) or 10% longer. To begin each trial participants had to press a key. After stimulus offset participants had to indicate via button press whether target or non-target duration was presented in a 2AFC manner. (B) Predictions for common neural mechanisms across different modalities (orange arrow for shorter duration, red for longer duration) or for different durations (green for auditory, blue for visual) based on correlation strengths of the variability in time estimation.

Figure 2

Figure 2

Behavioral performance strongly correlated across different modalities of temporal judgments. (A) Plots convey temporal estimation correlations between conditions either across modalities (top) or across durations (bottom). Colored arrows at the top of each plot correspond to the correlation arrows in Figure 1A. x and y axes indicate accuracy level (% correct) of specific conditions (condition name indicated on axis title). Each point depicts data from one participant (n = 31). Correlation strength and significance are indicated at the bottom right of each plot. See also Figures 6A–C. (B) Inter-individual variability in time estimation is strongly correlated across modalities (A) as depicted by thick arrows (orange for shorter durations, red for longer), indicating common neural mechanisms for time estimation across different modalities. Thin arrows (across durations) indicate weaker correlations.

Figure 3

Figure 3

Neural structural correlates of duration discrimination. For each of the experimental conditions, shown in red to yellow (blue) are those cortical loci where our analyses of cortical thickness revealed a significant positive (negative) correlation between cortical thickness and duration discrimination (p < 0.05, corrected) across the group of participants (n = 31). Aud2 (top left), Vis2 (top right), Aud12 (bottom left), Vis12 (bottom right). Data are shown overlaid onto an inflated template brain in a standard stereotactic space where sulci are represented in dark gray and gyri in light gray. Significant clusters are shown at _t_-values according to scale bar (bottom right) for visualization purposes (see Table 1 for further details). Note the common structural correlates for estimation of longer durations in right A1/PAC (primary auditory) and SII (secondary somatosensory) cortices for both longer visual and longer auditory durations. R, right; L, left; PHG, parahippocampal gyrus; Vis. Cort, visual cortex; lat, lateral; pos, posterior; vent, ventral.

Figure 4

Figure 4

Overlay of longer duration structural correlates on right A1/PAC (primary auditory) and SII (secondary somatosensory) cortices. Cortical loci where our analyses of cortical thickness revealed a significant positive correlation between cortical thickness and longer auditory [Aud12, **(A)**] or longer visual [Vis12, **(B)**] duration discrimination shown in red to bright yellow (_t_-values indicated on scale bar) superimposed on structures of A1/PAC and SII. A1/PAC and SII structures are denoted by colored contours according to the legend at the bottom (see Materials and Methods). Coronal (top) and sagittal (bottom) views. Arrows point to substantial portions of these structures that are correlated with longer duration discrimination ability, which are TE1.1 (PAC/A1, see orange arrows) and OP2–3 (SII, see blue and turquoise arrows). See also Figures 5A–C. R, right; L, left.

Figure 5

Figure 5

(A) Top: average T statistics of the Aud12 structural correlates _t_-map (as seen in Figure 3 bottom left and in Figure 4A). For each structure of A1/PAC (i.e., TE1.0, TE1.1, TE1.2) and for each structure of SII (i.e., OP1–OP4) the average is done over all the MNI coordinates that are highly likely (probability of 60–100%) to be in that structure according to the Juelich atlas (

http://www.fz-juelich.de/inm/and

SPM toolbox

http://www.fz-juelich.de/ime/spm\_anatomy\_toolbox

). Bottom: same analysis for the Vis12 structural correlates. The data show that the structural correlates of Aud12 and Vis12 are robust within TE1.1, OP2, and OP3 and are highly consistent and stable within these regions. Error bars, SD. (B) Same as (A) but over all the MNI coordinates that have a medium likelihood (probability of 40–60%) to be in the structures of A1/PAC and SII according to the Juelich atlas (see above). (C) Same as (A) but over all the MNI coordinates that have some likelihood (probability of 10–40%) of being in the structures of A1/PAC and SII according to the Juelich atlas (see above).

Figure 6

Figure 6

(A) Individual temporal discrimination ability for 12 s durations, as estimated by the original main experimental task and by a finer adaptive method (QUEST, see Materials and Methods). Each point in the scatter plots (left plot in threshold values, right plot same data in ms units) represents data from one participant (n = 13). The number of ms (right plot x axis) represents the duration difference needed for that individual to discriminate longer 12 s durations at a fixed accuracy level of 75%. Discrimination accuracy when the duration difference is fixed (discrimination of 12 from 13.2 s) is indicated on the y axis. The significant correlations found between these two measurements indicate on the reliability of the original main experimental task for estimating individual longer temporal discriminations ability. (B) Time discrimination performance vs. color discrimination performance: experimental design and results. Top: timeline and stimuli from two experimental trials in the experiment. Same paradigm was used for time discrimination task or color discrimination task (see Materials and Methods). The temporal task required discriminating between 12 and 13.2 s durations while ignoring the colored circles, the color task required discriminating between the colors of the last circle in the trial with the one preceding it (“same” or “different”). Expected responses according to the task are indicated on the top right corner. Both color and time task required attention and motivation throughout the task since the number of flashing circles and their appearances were unexpected [number of circles per trial varied across trials and stimulus appearances were asynchronous (different SOA)]. Bottom: correlation between individuals’ longer temporal duration discrimination performance and color discrimination performance is not significant. Each point in the scatter plots (left plot n = 13, right plot n = 12 without the outlier) represents one individual. (C) Correlation between shorter duration and longer duration discrimination abilities across all participants based on a finer adaptive QUEST procedure (see Materials and Methods). Each point in the scatter plots (left plot in threshold values, right plot same data in ms units) represents data from one participant. For shorter 2 s on y axis, and for longer 12 s on x axis, the number of ms (right plot) represents the duration difference needed for that individual to discriminate durations of that length at a fixed accuracy level of 75%. Thus, the duration difference for shorter durations does not correlate with the duration difference for longer durations, consistent with the results presented in Figure 2A bottom panels.

Figure 6

Figure 6

(A) Individual temporal discrimination ability for 12 s durations, as estimated by the original main experimental task and by a finer adaptive method (QUEST, see Materials and Methods). Each point in the scatter plots (left plot in threshold values, right plot same data in ms units) represents data from one participant (n = 13). The number of ms (right plot x axis) represents the duration difference needed for that individual to discriminate longer 12 s durations at a fixed accuracy level of 75%. Discrimination accuracy when the duration difference is fixed (discrimination of 12 from 13.2 s) is indicated on the y axis. The significant correlations found between these two measurements indicate on the reliability of the original main experimental task for estimating individual longer temporal discriminations ability. (B) Time discrimination performance vs. color discrimination performance: experimental design and results. Top: timeline and stimuli from two experimental trials in the experiment. Same paradigm was used for time discrimination task or color discrimination task (see Materials and Methods). The temporal task required discriminating between 12 and 13.2 s durations while ignoring the colored circles, the color task required discriminating between the colors of the last circle in the trial with the one preceding it (“same” or “different”). Expected responses according to the task are indicated on the top right corner. Both color and time task required attention and motivation throughout the task since the number of flashing circles and their appearances were unexpected [number of circles per trial varied across trials and stimulus appearances were asynchronous (different SOA)]. Bottom: correlation between individuals’ longer temporal duration discrimination performance and color discrimination performance is not significant. Each point in the scatter plots (left plot n = 13, right plot n = 12 without the outlier) represents one individual. (C) Correlation between shorter duration and longer duration discrimination abilities across all participants based on a finer adaptive QUEST procedure (see Materials and Methods). Each point in the scatter plots (left plot in threshold values, right plot same data in ms units) represents data from one participant. For shorter 2 s on y axis, and for longer 12 s on x axis, the number of ms (right plot) represents the duration difference needed for that individual to discriminate durations of that length at a fixed accuracy level of 75%. Thus, the duration difference for shorter durations does not correlate with the duration difference for longer durations, consistent with the results presented in Figure 2A bottom panels.

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