Spatial specificity of working memory representations in the early visual cortex

Abstract

Recent fMRI decoding studies have demonstrated that early retinotopic visual areas exhibit similar patterns of activity during the perception of a stimulus and during the maintenance of that stimulus in working memory. These findings provide support for the sensory recruitment hypothesis that the mechanisms underlying perception serve as a foundation for visual working memory. However, a recent study by Ester, Serences, and Awh (2009) found that the orientation of a peripheral grating maintained in working memory could be classified from both the contralateral and ipsilateral regions of the primary visual cortex (V1), implying that, unlike perception, feature-specific information was maintained in a nonretinotopic manner. Here, we evaluated the hypothesis that early visual areas can maintain information in a spatially specific manner and will do so if the task encourages the binding of feature information to a specific location. To encourage reliance on spatially specific memory, our experiment required observers to retain the orientations of two laterally presented gratings. Multivariate pattern analysis revealed that the orientation of each remembered grating was classified more accurately based on activity patterns in the contralateral than in the ipsilateral regions of V1 and V2. In contrast, higher extrastriate areas exhibited similar levels of performance across the two hemispheres. A time-resolved analysis further indicated that the retinotopic specificity of the working memory representation in V1 and V2 was maintained throughout the retention interval. Our results suggest that early visual areas provide a cortical basis for actively maintaining information about the features and locations of stimuli in visual working memory.

Keywords: decoding; fMRI; feature-based attention; imagery; pattern classification; visual short-term memory.

Figure 1

Classification accuracy for viewed gratings increases as a function of stimulus contrast in the contralateral visual cortex but falls around chance-level performance in the ipsilateral visual cortex. Adapted with permission from Tong et al. . Separate gratings were shown in each visual field with independent orientations on each block (45° or 135°) at one of three contrast levels. The left panel shows performance for contralateral hemispheres, which is significantly above chance for all visual areas at all contrast levels (all ps < 0.05, one-tailed t test). The right panel shows performance for the ipsilateral hemispheres, and all areas at all contrast levels failed to deviate significantly from chance with the single exception of V1 at 4% contrast, t(9) = 3.15, p < 0.05, uncorrected. Error bars indicate ±1 SEM based on data from 10 participants.

Figure 2

Trial structure. Two sample gratings were presented bilaterally at the beginning of each trial and were soon followed by two more gratings. A central cue of “1” or “2” then indicated which pair of gratings was to be retained during the subsequent retention interval. Following retention, a grating was presented in either the left or right position, rotated slightly clockwise or counterclockwise relative to the original sample grating presented in that location; a plaid stimulus appeared in the untested location. Participants indicated the direction of the orientation change within the response period.

Figure 3

Classification accuracy for orientations held in working memory. Left: Orientation classification performance for gratings presented to the ipsilateral and contralateral hemifields. Error bars denote standard errors; stars denote significant (p < 0.05) deviations from chance-level performance. Right: Contralateral advantage in classification as a function of the number of voxels used in each ROI. Asterisks denote statistically significant effects (p < 0.05); dots denote marginal significance (p < 0.10).

Figure 4

Time-resolved classification of remembered orientation for activity patterns in a combined V1–V4 ROI (left), an ROI combining visual areas V1 and V2 (middle), and an ROI combining areas V3 and V3AB/V4 (right). Pattern classifiers were trained and tested separately for each BOLD acquisition in each ROI. Error bars denote standard errors, asterisks denote significant differences between contralateral (blue curve) and ipsilateral (red curve) classification performance at each time point (p < 0.05, not corrected for multiple comparisons), and dots denote marginal significance (p < 0.10).