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. 2023 Oct 17;120(42):e2216942120.
doi: 10.1073/pnas.2216942120. Epub 2023 Oct 9.

Different roles of response covariability and its attentional modulation in the sensory cortex and posterior parietal cortex

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Different roles of response covariability and its attentional modulation in the sensory cortex and posterior parietal cortex

Yong Jiang et al. Proc Natl Acad Sci U S A. .

Abstract

The covariability of neural responses in the neuron population is highly relevant to the information encoding. Cognitive processes, such as attention, are found to modulate the covariability in the visual cortex to improve information encoding, suggesting the computational advantage of covariability modulation in the neural system. However, is the covariability modulation a general mechanism for enhanced information encoding throughout the information processing pathway, or only adopted in certain processing stages, depending on the property of neural representation? Here, with ultrahigh-field MRI, we examined the covariability, which was estimated by noise correlation, in different attention states in the early visual cortex and posterior parietal cortex (PPC) of the human brain, and its relationship to the quality of information encoding. Our results showed that while attention decreased the covariability to improve the stimulus encoding in the early visual cortex, covariability modulation was not observed in the PPC, where covariability had little impact on information encoding. Further, attention promoted the information flow between the early visual cortex and PPC, with an apparent emphasis on a flow from high- to low-dimensional representations, suggesting the existence of a reduction in the dimensionality of neural representation from the early visual cortex to PPC. Finally, the neural response patterns in the PPC could predict the amplitudes of covariability change in the early visual cortex, indicating a top-down control from the PPC to early visual cortex. Our findings reveal the specific roles of the sensory cortex and PPC during attentional modulation of covariability, determined by the complexity and fidelity of the neural representation in each cortical region.

Keywords: attention; covariability; early visual cortex; posterior parietal cortex.

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Conflict of interest statement

The authors declare no competing interest.

Figures

Fig. 1.
Fig. 1.
Experiment task and attentional modulation on neural responses in V1. (A) Behavioral task in the scanner. Participants were asked to identify the grating orientation (2° tilted either CW or CCW) at the attended location, which was indicated by the central cue. (B) ROI in the early visual cortex and PPC shown on the cortical surface. The color bar indicates the response significance to visual grating compared with baseline. The Inset shows the positioning of the slices of fMRI scan. (C) Averaged fMRI response time course of attended or unattended trials in V1. The black bar on the time axis indicates the presenting time of the grating stimulus. The gray shaded region indicates the peak duration of the response time courses, in which the fMRI signals were extracted as the neural responses for single trials to calculate the noise correlation in the voxel population. The colored shaded regions reflect ±1 SEM. (D) The averaged noise correlations of attended and unattended trials in the voxel population from V1. Error bars reflect ±1 SEM. ∗∗ indicates the paired t test with significance of P < 0.01.
Fig. 2.
Fig. 2.
Spatial and temporal profiles of covariability modulation. (A) The noise correlation of attended and unattended trials with voxel pairs grouped based on spatial distance. Similar attentional modulations were observed across different distance groups. (B) Schematic illustration of temporal filters being applied to the trial-to-trial neural response sequence. The x axis represents the trial number in the whole experiment. (C) The noise correlations in attended and unattended conditions in the high-passed sequences and low-passed sequences. Attention modulation of noise correlation was only observed in the fast fluctuation of trial-to-trial responses. ** indicates the paired t test with significance of P < 0.01. ∗ indicates the paired t test with significance of P < 0.05.
Fig. 3.
Fig. 3.
The relationship between covariability and information encoding in the V1 neural population. (A) Performances of stimulus orientation decoding in V1. The orientation information could be successfully decoded in the attended condition. (B) The noise correlations in voxel populations that were highly discriminative or weakly discriminative to stimulus orientations (CW vs. CCW, estimated by absolute t value). Attention significantly decreased the noise correlation in the high discriminative voxel population. (C) The neural responses of the voxel population with covariability removed (shuffled) showed better orientation decoding performances than that based on original neural responses. (D) The attention-induced noise correlation decrease was more prominent in the superficial layer in V1. Error bars reflect ±1 SEM. * indicates the significance of P < 0.05.
Fig. 4.
Fig. 4.
The neural modulation of attention in the pIPS. (A) Averaged fMRI response time courses of attended and unattended trials in the pIPS, with the shaded region indicts the peak period (same as that in V1). The colored shaded regions reflect ±1 SEM. (B) The averaged noise correlations of attended or unattended trials in the pIPS, with no significant difference being observed. (C) The noise correlation in different attention conditions and in voxel groups with different orientation discriminability. No significant difference was observed in either group. Error bars reflect ±1 SEM. (D) The removal of covariability had little benefit on orientation decoding performances.
Fig. 5.
Fig. 5.
Attentional effects on the information flow between the pIPS and V1. (A) The noise correlation between the pIPS and V1. Stronger correlations were observed in the attended than in unattended condition. Error bars reflect ±1 SEM. ∗ indicates the significance of P < 0.05. (B) The attentional effect (attended vs. unattended) on correlation between the pIPS and V1 estimated by CCA with different number of principal components included in each region. The solid lines indicate the significant clusters. The significant cluster located on the upper left suggests that attention boosted the information flow between the high-dimensional representation in V1 and low-dimensional representation in the pIPS. The dashed lines indicate the range of data presented in the figure below. (C) Attention enhanced correlation between neural representations in the pIPS and high dimensional representations in V1 (30 to 40 components). The result showed that the attention enhanced the correlation between two regions, and the attentional enhancement peaked at the first one or two components in the pIPS. With more pIPS components included, the correlation enhancement became lower.
Fig. 6.
Fig. 6.
Neural response bias in the pIPS predicting covariability changes in V1. The trials were grouped based on the contralateral bias of pIPS neural responses to the attended visual field (contralateral vs. ipsilateral). The attention-induced noise correlation decrease in V1 was observed only in the trial group with high contralateral bias of the pIPS (left column). Such effect was most prominent in the superficial layer of the pIPS (right column). Error bars reflect ±1 SEM. ** indicates the significance of P < 0.01. * indicates the significance of P < 0.05.

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