Visual Working Memory in Human Cortex

Abstract

Visual working memory (VWM) is the ability to maintain visual information in a readily available and easily updated state. Converging evidence has revealed that VWM capacity is limited by the number of maintained objects, which is about 3 - 4 for the average human. Recent work suggests that VWM capacity is also limited by the resolution required to maintain objects, which is tied to the objects’ inherent complexity. Electroencephalogram (EEG) studies using the Contralateral Delay Activity (CDA) paradigm have revealed that cortical representations of VWM are at a minimum loosely organized like the primary visual system, such that the left side of space is represented in the right hemisphere, and vice versa. Recent functional magnetic resonance imaging (fMRI) work shows that the number of objects is maintained by representations in the inferior intraparietal sulcus (IPS) along dorsal parietal cortex, whereas the resolution of these maintained objects is subserved by the superior IPS and the lateral occipital complex (LOC). These areas overlap with recently-discovered, retinotopically-organized visual field maps (VFMs) spanning the IPS (IPS-0/1/2/3/4/5), and potentially maps in lateral occipital cortex, such as LO-1/2, and/or TO-1/2 (hMT+). Other fMRI studies have implicated early VFMs in posterior occipital cortex, suggesting that visual areas V1-hV4 are recruited to represent information in VWM. Insight into whether and how these VFMs subserve VWM may illuminate the nature of VWM. In addition, understanding the nature of these maps may allow a greater investigation into individual differences among subjects and even between hemispheres within subjects.

Share and Cite:

Barton, B. & Brewer, A. (2013). Visual Working Memory in Human Cortex. Psychology, 4, 655-662. doi: 10.4236/psych.2013.48093.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Alvarez, G. A., & Cavanagh, P. (2004). The capacity of visual shortterm memory is set both by visual information load and by number of objects. Psychological Science, 15, 106-111. doi:10.1111/j.0963-7214.2004.01502006.x
[2] Amano, K., Wandell, B. A. et al. (2009). Visual field maps, population receptive field sizes, and visual field coverage in the human MT+ complex. Journal of Neurophysiology, 102, 2704-2718. doi:10.1152/jn.00102.2009
[3] Anderson, D. E., Vogel, E. K. et al. (2011). Precision in visual working memory reaches a stable plateau when individual item limits are exceeded. Journal of Neuroscience, 31, 1128-1138. doi:10.1523/JNEUROSCI.4125-10.2011
[4] Awh, E., Barton, B. et al. (2007). Visual working memory represents a fixed number of items regardless of complexity. Psychological Science, 18, 622-628. doi:10.1111/j.1467-9280.2007.01949.x
[5] Baddeley, A. (1996). Exploring the central executive. The Quarterly Journal of Experimental Psychology Section A: Human Experimental Psychology, 49, 5-28.
[6] Baddeley, A. (2000). The episodic buffer: A new component of working memory? Trends in Cognitive Sciences, 4, 417-423. doi:10.1016/S1364-6613(00)01538-2
[7] Baddeley, A. (2003). Working memory: Looking back and looking forward. Nature Reviews Neuroscience, 4, 829-839. doi:10.1038/nrn1201
[8] Baddeley, A. D., & Hitch, G. (1974). Working memory. In H. B. Gordon (Ed.), Psychology of learning and motivation (Vol. 8, pp. 47-89). Waltham, MA: Academic Press.
[9] Baizer, J. S., Ungerleider, L. G. et al. (1991). Organization of visual inputs to the inferior temporal and posterior parietal cortex in macaques. Journal of Neuroscience, 11, 168-190.
[10] Barton, B., & Brewer, A. A. (2010). Visual working memory capacity in retinotopic cortex: Number, resolution, and population receptive fields. Journal of Vision, 10, 729. doi:10.1167/10.7.729
[11] Barton, B., Ester, E. F. et al. (2009). Discrete resource allocation in visual working memory. Journal of Experimental Psychology: Human Perception and Performance, 35, 1359-1367. doi:10.1037/a0015792
[12] Bays, P. M., & Husain, M. (2008). Dynamic shifts of limited working memory resources in human vision. Science, 321, 851-854. doi:10.1126/science.1158023
[13] Bays, P. M., Gorgoraptis, N. et al. (2011). Temporal dynamics of encoding, storage, and reallocation of visual working memory. Journal of Vision, 11, Article 6. doi:10.1167/11.10.6
[14] Bays, P. M., Catalao, R. F. et al. (2009). The precision of visual working memory is set by allocation of a shared resource. Journal of Vision, 9, Article 7.
[15] Blackwood, D. H., & Muir, W. J. (1990). Cognitive brain potentials and their application. British Journal of Psychiatry Supplements, 9, 96-101.
[16] Brewer, A. A., & Barton, B. (2012). Visual field map organization in human visual cortex. In S. Molotchnikoff (Ed.), Visual Cortex, InTech, 29-60.
[17] Brewer, A. A., Liu, J. et al. (2005). Visual field maps and stimulus selectivity in human ventral occipital cortex. Nature Neuroscience, 8, 1102-1109. doi:10.1038/nn1507
[18] Brewer, A. A., Press, W. A. et al. (2002). Visual areas in macaque cortex measured using functional magnetic resonance imaging. Journal of Neuroscience, 22, 10416-10426.
[19] Cavanagh, P., & Alvarez, G. A. (2005). Tracking multiple targets with multifocal attention. Trends in Cognitive Sciences, 9, 349-354. doi:10.1016/j.tics.2005.05.009
[20] Chen, Y., & Parrish, T. B. (2009). Caffeine’s effects on cerebrovascular reactivity and coupling between cerebral blood flow and oxygen metabolism. Neuroimage, 44, 647-652. doi:10.1016/j.neuroimage.2008.09.057
[21] Clark, V. P., Fan, S. et al. (1994). Identification of early visual evoked potential generators by retinotopic and topographic analyses. Human Brain Mapping, 2, 170-187. doi:10.1002/hbm.460020306
[22] Cowan, N. (2001). The magical number 4 in short-term memory: A reconsideration of mental storage capacity. Behavioral and Brain Sciences, 24, 87-114. doi:10.1017/S0140525X01003922
[23] Culham, J. C., & Kanwisher, N. G. (2001). Neuroimaging of cognitive functions in human parietal cortex. Current Opinion in Neurobiology, 11, 157-163. doi:10.1016/S0959-4388(00)00191-4
[24] Culham, J. C., Cavanagh, P. et al. (2001). Attention response functions: Characterizing brain areas using fMRI activation during parametric variations of attentional load. Neuron, 32, 737-745. doi:10.1016/S0896-6273(01)00499-8
[25] Culham, J. C., Brandt, S. A. et al. (1998). Cortical fMRI activation produced by attentive tracking of moving targets. Journal of Neurophysiology, 80, 2657-2670.
[26] Curtis, C. E., & D’Esposito, M. (2003). Persistent activity in the prefrontal cortex during working memory. Trends in Cognitive Sciences, 7, 415-423. doi:10.1016/S1364-6613(03)00197-9
[27] D’Esposito, M., & Postle, B. R. (1999). The dependence of span and delayed-response performance on prefrontal cortex. Neuropsychologia, 37, 1303-1315. doi:10.1016/S0028-3932(99)00021-4
[28] DeYoe, E. A., Carman, G. J. et al. (1996). Mapping striate and extrastriate visual areas in human cerebral cortex. Proceedings of the National Academy of Sciences of the United States of America, 93, 2382-2386. doi:10.1073/pnas.93.6.2382
[29] Dougherty, R. F., Koch, V. M. et al. (2003). Visual field representations and locations of visual areas V1/2/3 in human visual cortex. Journal of Vision, 3, 586-598. doi:10.1167/3.10.1
[30] Drew, T., & Vogel, E. K. (2008). Neural measures of individual differences in selecting and tracking multiple moving objects. Journal of Neuroscience, 28, 4183-4191. doi:10.1523/JNEUROSCI.0556-08.2008
[31] Drew, T. W., McCollough, A. W. et al. (2006). Event-related potential measures of visual working memory. Clinical EEG & Neuroscience, 37, 286-291. doi:10.1177/155005940603700405
[32] Dumoulin, S. O., & Wandell, B. A. (2008). Population receptive field estimates in human visual cortex. Neuroimage, 39, 647-660. doi:10.1016/j.neuroimage.2007.09.034
[33] Engel, S. A. (2012). The development and use of phase-encoded functional MRI designs. Neuroimage, 62, 1195-1200. doi:10.1016/j.neuroimage.2011.09.059
[34] Engel, S. A., Rumelhart, D. E. et al. (1994). fMRI of human visual cortex. Nature, 369, 525. doi:10.1038/369525a0
[35] Engel, S. A., Glover, G. H. et al. (1997). Retinotopic organization in human visual cortex and the spatial precision of functional MRI. Cereb Cortex, 7, 181-192. doi:10.1093/cercor/7.2.181
[36] Ester, E. F., Anderson, D. E. et al. (2013). A neural measure of precision in visual working memory. Journal of Cognitive Neuroscience, 25, 754-761. doi:10.1162/jocn_a_00357
[37] Felleman, D. J., & Van Essen, D. C. (1991). Distributed hierarchical processing in the primate cerebral cortex. Cerebral Cortex, 1, 1-47. doi:10.1093/cercor/1.1.1
[38] Gao, Z., Li, J. et al. (2009). Storing fine detailed information in visual working memory—Evidence from event-related potentials. Journal of Vision, 9, 1-12. doi:10.1167/9.7.17
[39] Harrison, S. A., & Tong, F. (2009). Decoding reveals the contents of visual working memory in early visual areas. Nature, 458, 632-635. doi:10.1038/nature07832
[40] Irwin, D. E. (1992). Memory for position and identity across eye movements. Journal of Experimental Psychology, 18, 307-317.
[41] Jonides, J., Smith, E. E. et al. (1993). Spatial working memory in humans as revealed by PET. Nature, 363, 623-625. doi:10.1038/363623a0
[42] Keshvari, S., van den Berg, R. et al. (2013). No evidence for an item limit in change detection. PLoS Computational Biology, 9, 1. doi:10.1371/journal.pcbi.1002927
[43] Kolster, H., Peeters, R. et al. (2010). The retinotopic organization of the human middle temporal area MT/V5 and its cortical neighbors. The Journal of Neuroscience, 30, 9801-9820. doi:10.1523/JNEUROSCI.2069-10.2010
[44] Konen, C. S., & Kastner, S. (2008). Representation of eye movements and stimulus motion in topographically organized areas of human posterior parietal cortex. The Journal of Neuroscience, 28, 8361-8375. doi:10.1523/JNEUROSCI.1930-08.2008
[45] Larsson, J., & Heeger, D. J. (2006). Two retinotopic visual areas in human lateral occipital cortex. The Journal of Neuroscience, 26, 13128-13142. doi:10.1523/JNEUROSCI.1657-06.2006
[46] Logothetis, N. K., & Wandell, B. A. (2004). Interpreting the BOLD signal. Annual Review of Physiology, 66, 735-769. doi:10.1146/annurev.physiol.66.082602.092845
[47] Logothetis, N. K., Pauls, J. et al. (2001). Neurophysiological investigation of the basis of the fMRI signal. Nature, 412, 150-157. doi:10.1038/35084005
[48] Luck, S. J. (1999). Direct and indirect integration of event-related potentials, functional magnetic resonance images, and single-unit recordings. Human Brain Mapping, 8, 115-201. doi:10.1002/(SICI)1097-0193(1999)8:2/3<115::AID-HBM8>3.0.CO;2-3
[49] Luck, S. J., & Vogel, E. K. (1997). The capacity of visual working memory for features and conjunctions. Nature, 390, 279-281. doi:10.1038/36846
[50] Luck, S. J., Woodman, G. F. et al. (2000). Event-related potential studies of attention. Trends in Cognitive Sciences, 4, 432-440. doi:10.1016/S1364-6613(00)01545-X
[51] McCollough, A. W., Machizawa, M. G. et al. (2007). Electrophysiological measures of maintaining representations in visual working memory. Cortex, 43, 77-94. doi:10.1016/S0010-9452(08)70447-7
[52] Morel, A., & Bullier J. (1990). Anatomical segregation of two cortical visual pathways in the macaque monkey. Visual Neuroscience, 4, 555-578. doi:10.1017/S0952523800005769
[53] Ogawa, S., Tank, D. et al. (1992). Intrinsic signal changes accompanying sensory stimulation: Functional brain mapping with magnetic resonance imaging. Proceedings of the National Academy of Sciences of the United States of America, 89, 591-5955. doi:10.1073/pnas.89.13.5951
[54] Pashler, H. (1988). Familiarity and visual change detection. Perception & Psychophysics, 44, 369-378. doi:10.3758/BF03210419
[55] Poldrack, R. A., Fletcher, P. C. et al. (2008). Guidelines for reporting an fMRI study. Neuroimage, 40, 409-414. doi:10.1016/j.neuroimage.2007.11.048
[56] Postle, B. R. (2006). Working memory as an emergent property of the mind and brain. Neuroscience, 139, 23-38. doi:10.1016/j.neuroscience.2005.06.005
[57] Postle, B. R., Awh, E. et al. (2004). The where and how of attentionbased rehearsal in spatial working memory. Brain Research. Cognitive Brain Research, 20, 194-205. doi:10.1016/j.cogbrainres.2004.02.008
[58] Postle, B. R., Zarahn, E. et al. (2000). Using event-related fMRI to assess delay-period activity during performance of spatial and nonspatial working memory tasks. Brain Research Protocols, 5, 57-66. doi:10.1016/S1385-299X(99)00053-7
[59] Postle, B. R., Berger, J. S. et al. (2000). Activity in human frontal cortex associated with spatial working memory and saccadic behavior. Journal of Cognitive Neuroscience, 12, 2-14. doi:10.1162/089892900564028
[60] Press, W. A., Brewer, A. A. et al. (2001). Visual areas and spatial summation in human visual cortex. Vision Research, 41, 1321-1332. doi:10.1016/S0042-6989(01)00074-8
[61] Pylyshyn, Z. W., & Storm, R. W. (1988). Tracking multiple independent targets: Evidence for a parallel tracking mechanism. Spatial Vision, 3, 179-197. doi:10.1163/156856888X00122
[62] Roth, J. K., Serences, J. T. et al. (2006). Neural system for controlling the contents of object working memory in humans. Cerebral Cortex, 16, 1595-1603. doi:10.1093/cercor/bhj096
[63] Rouder, J. N., Morey, R. D. et al. (2008). An assessment of fixed-capacity models of visual working memory. Proceedings of the National Academy of Sciences of the United States of America, 105, 5975-5979. doi:10.1073/pnas.0711295105
[64] Rypma, B., Berger, J. S. et al. (2002). The influence of working-memory demand and subject performance on prefrontal cortical activity. Journal of Cognitive Neuroscience, 14, 721-731. doi:10.1162/08989290260138627
[65] Schira, M. M., Tyler, C. W. et al. (2009). The foveal confluence in human visual cortex. The Journal of Neuroscience, 29, 9050-9058. doi:10.1523/JNEUROSCI.1760-09.2009
[66] Schridde, U., Khubchandani, M. et al. (2008). Negative BOLD with large increases in neuronal activity. Cerebral Cortex, 18, 1814-1827. doi:10.1093/cercor/bhm208
[67] Schummers, J., Yu, H. et al. (2008). Tuned responses of astrocytes and their influence on hemodynamic signals in the visual cortex. Science, 320, 1638-1643. doi:10.1126/science.1156120
[68] Scolari, M., Vogel, E. K. et al. (2008). Perceptual expertise enhances the resolution but not the number of representations in working memory. Psychonomic Bulletin and Review, 15, 215-222. doi:10.3758/PBR.15.1.215
[69] Serences, J. T. (2004). A comparison of methods for characterizing the event-related BOLD timeseries in rapid fMRI. Neuroimage, 21, 1690-1700. doi:10.1016/j.neuroimage.2003.12.021
[70] Sereno, M. I., & Tootell, R. B. (2005). From monkeys to humans: What do we now know about brain homologies? Current Opinion in Neurobiology, 15, 135-144. doi:10.1016/j.conb.2005.03.014
[71] Sereno, M. I., Dale, A. M. et al. (1995). Borders of multiple human visual areas in humans revealed by functional MRI. Science, 268, 889-893. doi:10.1126/science.7754376
[72] Sereno, M. I., Pitzalis, S. et al. (2001). Mapping of contralateral space in retinotopic coordinates by a parietal cortical area in humans. Science, 294, 1350-1354. doi:10.1126/science.1063695
[73] Shmuel, A., Augath, M. et al. (2006). Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1. Nature Neuroscience, 9, 569-577. doi:10.1038/nn1675
[74] Silver, M. A., Ress, D. et al. (2005). Topographic maps of visual spatial attention in human parietal cortex. Journal of Neurophysiology, 94, 1358-1371. doi:10.1152/jn.01316.2004
[75] Simons, D. J., & Ambinder, M. S. (2005). Change blindness. Current Directions in Psychological Science, 14, 44-48. doi:10.1111/j.0963-7214.2005.00332.x
[76] Sligte, I. G., Scholte, H. S. et al. (2008). Are there multiple visual short-term memory stores? PLoS One, 3, e1699. doi:10.1371/journal.pone.0001699
[77] Sligte, I. G., Scholte, H. S. et al. (2009). V4 Activity predicts the strength of visual short-term memory representations. Journal of Neuroscience, 29, 7432-7438. doi:10.1523/JNEUROSCI.0784-09.2009
[78] Smith, A. T., Greenlee, M. W. et al. (1998). The processing of first- and second-order motion in human visual cortex assessed by functional magnetic resonance imaging (fMRI). The Journal of Neuroscience, 18, 3816-3830.
[79] Sperling, G. (1960). The information available in brief visual presentations. Psychological Monographs: General and Applied, 74, 1-29. doi:10.1037/h0093759
[80] Sur, S., & Sinha, V. K. (2009). Event-related potential: An overview. Indian Journal of Psychiatry, 18, 70-73. doi:10.4103/0972-6748.57865
[81] Swisher, J. D., Halko, M. A. et al. (2007). Visual topography of human intraparietal sulcus. The Journal of Neuroscience, 27, 5326-5337. doi:10.1523/JNEUROSCI.0991-07.2007
[82] Todd, J. J., & Marois, R. (2004). Capacity limit of visual short-term memory in human posterior parietal cortex. Nature, 428, 751-754. doi:10.1038/nature02466
[83] Todd, J. J., & Marois, R. (2005). Posterior parietal cortex activity predicts individual differences in visual short-term memory capacity. Cognitive, Affective, & Behavioral Neuroscience, 5, 144-155. doi:10.3758/CABN.5.2.144
[84] Tootell, R. B., Mendola, J. D. et al. (1997). Functional analysis of V3A and related areas in human visual cortex. The Journal of Neuroscience, 17, 7060-7078. doi:10.1016/S0896-6273(00)80659-5
[85] Tootell, R. B., Hadjikhani, N. et al. (1998). The retinotopy of visual spatial attention. Neuron, 21, 1409-1422.
[86] Tootell, R. B., Hadjikhani, N. K. et al. (1998). Functional analysis of primary visual cortex (V1) in humans. Proceedings of the National Academy of Sciences of the United States of America, 95, 811-817. doi:10.1073/pnas.95.3.811
[87] Van Essen, D. C., Newsome, W. T. et al. (1984). The visual field representation in striate cortex of the macaque monkey: Asymmetries, anisotropies, and individual variability. Vision Research, 24, 429-448. doi:10.1016/0042-6989(84)90041-5
[88] Vogel, E. K., & Machizawa, M. G. (2004). Neural activity predicts individual differences in visual working memory capacity. Nature, 428, 748-751. doi:10.1038/nature02447
[89] Vogel, E. K., McCollough, A. W. et al. (2005). Neural measures reveal individual differences in controlling access to working memory. Nature, 438, 500-503. doi:10.1038/nature04171
[90] Vogel, E. K., Woodman, G. F. et al. (2001). Storage of features, conjunctions and objects in visual working memory. Journal of Experimental Psychology: Human Perception and Performance, 27, 92-114. doi:10.1037/0096-1523.27.1.92
[91] Wade, A. R., Brewer, A. A. et al. (2002). Functional measurements of human ventral occipital cortex: Retinotopy and colour. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 357, 963-973. doi:10.1098/rstb.2002.1108
[92] Wandell, B. A. (1999). Computational neuroimaging of human visual cortex. Annual Review of Neuroscience, 22, 145-173. doi:10.1146/annurev.neuro.22.1.145
[93] Wandell, B. A., & Winawer, J. (2011). Imaging retinotopic maps in the human brain. Vision Research, 51, 718-737. doi:10.1016/j.visres.2010.08.004
[94] Wandell, B. A., Dumoulin, S. O. et al. (2007). Visual field maps in human cortex. Neuron, 56, 366-383. doi:10.1016/j.neuron.2007.10.012
[95] Xu, Y., & Chun, M. M. (2006). Dissociable neural mechanisms supporting visual short-term memory for objects. Nature, 440, 91-95. doi:10.1038/nature04262
[96] Xu, Y., & Chun, M. M. (2007). Visual grouping in human parietal cortex. Proceedings of the National Academy of Sciences of the United States of America, 104, 18766-18771. doi:10.1073/pnas.0705618104
[97] Xu, Y., & Chun, M. M. (2009). Selecting and perceiving multiple visual objects. Trends in Cognitive Sciences, 13, 167-174. doi:10.1016/j.tics.2009.01.008
[98] Zhang, W., & Luck, S. J. (2008). Discrete fixed-resolution representations in visual working memory. Nature, 453, 233-235. doi:10.1038/nature06860

Copyright © 2024 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.