Abstract
Working memory refers to a system involved in the online maintenance and manipulation of information in the absence of external input. Due to the importance of working memory in higher-level cognition, a wealth of neuroscience studies has investigated its neural basis. These studies have often led to conflicting viewpoints regarding the importance of the prefrontal cortex (PFC) and posterior sensory cortices. Here, we review evidence for each position. We suggest that the relative contributions of the PFC and sensory cortices to working memory can be understood with respect to processing demands. We argue that procedures that minimize processing demands lead to increased importance of sensory representations, while procedures that permit transformational processing lead to representational abstraction that relies on the PFC. We suggest that abstract PFC representations support top-down control over posterior representations while also providing bottom-up inputs into higher-level cognitive processing. Although a number of contemporary studies have studied working memory while using procedures that minimize the role of the PFC, we argue that consideration of the PFC is critical for our understanding of working memory and higher-level cognition more generally.
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References
Atkins AS, Berman MG, Reuter-Lorenz PA, Lewis RL, Jonides J (2011) Resolving semantic and proactive interference in memory over the short-term. Mem Cogn 39:806–817
Atkinson RC, Shiffrin RM (1968) Human memory: a proposed system and its control processes. Psychol Learn Motiv 2:89–195
Azuar C, Reyes P, Slachevsky A, Volle E, Kinkingnehun S, Kouneiher F, Bravo E, Dubois B, Koechlin E, Levy R (2014) Testing the model of caudo-rostral organization of cognitive control in the human with frontal lesions. Neuroimage 84:1053–1060
Baddeley AD (1986) Working memory. Oxford University Press, Oxford
Baddeley A (2012) Working memory: theories, models, and controversies. Annu Rev Psychol 63:1–29
Baddeley AD, Hitch GJ (1974) Working memory. In: Bower GH (ed) The psychology of learning and motivation. Academic Press, New York, pp 47–89
Badre D (2008) Cognitive control, hierarchy, and the rostro-caudal organization of the frontal lobes. Trends Cogn Sci 12:193–200
Badre D, D’Esposito M (2007) Functional magnetic resonance imaging evidence for a hierarchical organization of the prefrontal cortex. J Cogn Neurosci 19:2082–2099
Badre D, D’Esposito M (2009) Is the rostro-caudal axis of the frontal lobe hierarchical? Nat Rev Neurosci 10:659–669
Badre D, Hoffman J, Cooney JW, D’Esposito M (2009) Hierarchical cognitive control deficits following damage to the human frontal lobe. Nat Neurosci 12:515–522
Badre D, Kayser AS, D’Esposito M (2010) Frontal cortex and the discovery of abstract action rules. Neuron 66:315–326
Bays PM (2014) Noise in neural populations accounts for errors in working memory. J Neurosci Official J Soc Neurosci 34:3632–3645
Carpenter PA, Just MA, Shell P (1990) What one intelligence test measures: a theoretical account of the processing in the raven progressive matrices test. Psychol Rev 97:404–431
Chafee MV, Goldman-Rakic PS (1998) Matching patterns of activity in primate prefrontal area 8a and parietal area 7ip neurons during a spatial working memory task. J Neurophysiol 79:2919–2940
Chen AJ, Britton M, Turner GR, Vytlacil J, Thompson TW, D’Esposito M (2012) Goal-directed attention alters the tuning of object-based representations in extrastriate cortex. Front Hum Neurosci 6:187
Christophel TB, Hebart MN, Haynes JD (2012) Decoding the contents of visual short-term memory from human visual and parietal cortex. J Neurosci Official J Soc Neurosci 32:12983–12989
Clapp WC, Rubens MT, Gazzaley A (2010) Mechanisms of working memory disruption by external interference. Cereb Cortex 20:859–872
Cohen JD, Perlstein WM, Braver TS, Nystrom LE, Noll DC, Jonides J, Smith EE (1997) Temporal dynamics of brain activation during a working memory task. Nature 386:604–608
Constantinidis C, Steinmetz MA (1996) Neuronal activity in posterior parietal area 7a during the delay periods of a spatial memory task. J Neurophysiol 76:1352–1355
Courtney SM, Petit L, Maisog JM, Ungerleider LG, Haxby JV (1998) An area specialized for spatial working memory in human frontal cortex. Science 279:1347–1351
Curtis CE, D’Esposito M (2003) Persistent activity in the prefrontal cortex during working memory. Trends Cogn Sci 7:415–423
Curtis CE, Rao VY, D’Esposito M (2004) Maintenance of spatial and motor codes during oculomotor delayed response tasks. J Neurosci Official J Soc Neurosci 24:3944–3952
Daneman M, Carpenter PA (1980) Individual differences in working memory and reading. J Verbal Learn Verbal Behav 19:450–466
Daneman M, Merikle PM (1996) Working memory and language comprehension: a meta-analysis. Psychon Bull Rev 3:422–433
D’Esposito M (2007) From cognitive to neural models of working memory. Philos Trans R Soc Lond B Biol Sci 362:761–772
Druzgal TJ, D’Esposito M (2001) Activity in fusiform face area modulated as a function of working memory load. Brain Res Cogn Brain Res 10:355–364
Druzgal TJ, D’Esposito M (2003) Dissecting contributions of prefrontal cortex and fusiform face area to face working memory. J Cogn Neurosci 15:771–784
Duncan J, Owen AM (2000) Common regions of the human frontal lobe recruited by diverse cognitive demands. Trends Neurosci 23:475–483
Emrich SM, Riggall AC, Larocque JJ, Postle BR (2013) Distributed patterns of activity in sensory cortex reflect the precision of multiple items maintained in visual short-term memory. J Neurosci Official J Soc Neurosci 33:6516–6523
Erickson MA, Maramara LA, Lisman J (2010) A single brief burst induces GluR1-dependent associative short-term potentiation: a potential mechanism for short-term memory. J Cogn Neurosci 22:2530–2540
Ester EF, Anderson DE, Serences JT, Awh E (2013) A neural measure of precision in visual working memory. J Cogn Neurosci 25:754–761
Freedman DJ, Riesenhuber M, Poggio T, Miller EK (2003) A comparison of primate prefrontal and inferior temporal cortices during visual categorization. J Neurosci Official J Soc Neurosci 23:5235–5246
Fukuda K, Vogel E, Mayr U, Awh E (2010) Quantity, not quality: the relationship between fluid intelligence and working memory capacity. Psychon Bull Rev 17:673–679
Funahashi S, Bruce CJ, Goldman-Rakic PS (1989) Mnemonic coding of visual space in the monkey’s dorsolateral prefrontal cortex. J Neurophysiol 61:331–349
Funahashi S, Bruce CJ, Goldman-Rakic PS (1993) Dorsolateral prefrontal lesions and oculomotor delayed-response performance: evidence for mnemonic “scotomas”. J Neurosci Official J Soc Neurosci 13:1479–1497
Fuster JM, Alexander GE (1971) Neuron activity related to short-term memory. Science 173:652–654
Fuster JM, Jervey JP (1982) Neuronal firing in the inferotemporal cortex of the monkey in a visual memory task. J Neurosci Official J Soc Neurosci 2:361–375
Garcia JO, Srinivasan R, Serences JT (2013) Near-real-time feature-selective modulations in human cortex. Curr Biol CB 23:515–522
Goldman PS, Nauta WJ (1977) Columnar distribution of cortico-cortical fibers in the frontal association, limbic, and motor cortex of the developing rhesus monkey. Brain Res 122:393–413
Goldman-Rakic PS (1987) Circuitry of the primate prefrontal cortex and the regulation of behavior by representational memory. In: Plum F, Mountcastle VB (eds) Handbook of physiology. American Physiological Society, Bethseda, pp 373–417
Goldman-Rakic PS (1995) Cellular basis of working memory. Neuron 14:477–485
Harrison SA, Tong F (2009) Decoding reveals the contents of visual working memory in early visual areas. Nature 458:632–635
Jerde TA, Merriam EP, Riggall AC, Hedges JH, Curtis CE (2012) Prioritized maps of space in human frontoparietal cortex. J Neurosci Official J Soc Neurosci 32:17382–17390
Jha AP, Fabian SA, Aguirre GK (2004) The role of prefrontal cortex in resolving distractor interference. Cogn Affect Behav Neurosci 4:517–527
Jonides J, Lacey S, Nee D (2005) Processes of working memory in mind and brain. Curr Dir Psychol Sci 14:2–5
Jonides J, Lewis RL, Nee DE, Lustig CA, Berman MG, Moore KS (2008) The mind and brain of short-term memory. Annu Rev Psychol 59:193–224
Just MA, Carpenter PA (1992) A capacity theory of comprehension—individual-differences in working memory. Psychol Rev 99:122–149
Kanwisher N, McDermott J, Chun MM (1997) The fusiform face area: a module in human extrastriate cortex specialized for face perception. J Neurosci 17:4302–4311
Koechlin E, Ody C, Kouneiher F (2003) The architecture of cognitive control in the human prefrontal cortex. Science 302:1181–1185
Kubota K, Niki H (1971) Prefrontal cortical unit activity and delayed alternation performance in monkeys. J Neurophysiol 34:337–347
Lara AH, Wallis JD (2014) Executive control processes underlying multi-item working memory. Nat Neurosci 17:876–883
LaRocque JJ, Lewis-Peacock JA, Drysdale AT, Oberauer K, Postle BR (2013) Decoding attended information in short-term memory: an EEG study. J Cogn Neurosci 25:127–142
Larocque JJ, Lewis-Peacock JA, Postle BR (2014) Multiple neural states of representation in short-term memory? It’s a matter of attention. Front Hum Neurosci 8:5
Lee TG, D’Esposito M (2012) The dynamic nature of top-down signals originating from prefrontal cortex: a combined fMRI-TMS study. J Neurosci Official J Soc Neurosci 32:15458–15466
Lee SH, Kravitz DJ, Baker CI (2013) Goal-dependent dissociation of visual and prefrontal cortices during working memory. Nat Neurosci 16:997–999
Lepsien J, Nobre AC (2007) Attentional modulation of object representations in working memory. Cereb Cortex 17:2072–2083
Levy R, Goldman-Rakic PS (2000) Segregation of working memory functions within the dorsolateral prefrontal cortex. Exp Brain Res 133:23–32
Lewis-Peacock JA, Postle BR (2008) Temporary activation of long-term memory supports working memory. J Neurosci Official J Soc Neurosci 28:8765–8771
Lewis-Peacock JA, Drysdale AT, Oberauer K, Postle BR (2012) Neural evidence for a distinction between short-term memory and the focus of attention. J Cogn Neurosci 24:61–79
Lewis-Peacock JA, Drysdale AT, Postle BR (2014) Neural evidence for the flexible control of mental representations. Cereb Cortex
Linden DE, Oosterhof NN, Klein C, Downing PE (2012) Mapping brain activation and information during category-specific visual working memory. J Neurophysiol 107:628–639
Luck SJ, Vogel EK (2013) Visual working memory capacity: from psychophysics and neurobiology to individual differences. Trends Cogn Sci 17:391–400
Ma WJ, Husain M, Bays PM (2014) Changing concepts of working memory. Nat Neurosci 17:347–356
Machizawa MG, Driver J (2011) Principal component analysis of behavioural individual differences suggests that particular aspects of visual working memory may relate to specific aspects of attention. Neuropsychologia 49:1518–1526
Mendoza-Halliday D, Torres S, Martinez-Trujillo JC (2014) Sharp emergence of feature-selective sustained activity along the dorsal visual pathway. Nat Neurosci 17:1255–1262
Meyers EM, Freedman DJ, Kreiman G, Miller EK, Poggio T (2008) Dynamic population coding of category information in inferior temporal and prefrontal cortex. J Neurophysiol 100:1407–1419
Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24:167–202
Miller EK, Erickson CA, Desimone R (1996) Neural mechanisms of visual working memory in prefrontal cortex of the macaque. J Neurosci 16:5154–5167
Miller BT, Vytlacil J, Fegen D, Pradhan S, D’Esposito M (2011) The prefrontal cortex modulates category selectivity in human extrastriate cortex. J Cogn Neurosci 23:1–10
Miyashita Y, Chang HS (1988) Neuronal correlate of pictorial short-term memory in the primate temporal cortex. Nature 331:68–70
Mongillo G, Barak O, Tsodyks M (2008) Synaptic theory of working memory. Science 319:1543–1546
Nee DE, Brown JW (2012) Rostral-caudal gradients of abstraction revealed by multi-variate pattern analysis of working memory. Neuroimage 63:1285–1294
Nee DE, Brown JW (2013) Dissociable frontal-striatal and frontal-parietal networks involved in updating hierarchical contexts in working memory. Cereb Cortex 23:2146–2158
Nee DE, Jonides J (2011) Dissociable contributions of prefrontal cortex and the hippocampus to short-term memory: evidence for a 3-state model of memory. Neuroimage 54:1540–1548
Nee DE, Jonides J (2013a) Trisecting representational states in short-term memory. Front Hum Neurosci 7:796
Nee DE, Jonides J (2013b) Neural evidence for a 3-state model of visual short-term memory. Neuroimage 74:1–11
Nee DE, Brown JW, Askren MK, Berman MG, Demiralp E, Krawitz A, Jonides J (2013) A meta-analysis of executive components of working memory. Cereb Cortex 23:264–282
Nee DE, Jahn A, Brown JW (2014) Prefrontal cortex organization: dissociating effects of temporal abstraction, relational abstraction, and integration with FMRI. Cereb Cortex 24:2377–2387
Niendam TA, Laird AR, Ray KL, Dean YM, Glahn DC, Carter CS (2012) Meta-analytic evidence for a superordinate cognitive control network subserving diverse executive functions. Cogn Affect Behav Neurosci 12:241–268
Norman KA, Polyn SM, Detre GJ, Haxby JV (2006) Beyond mind-reading: multi-voxel pattern analysis of fMRI data. Trends Cogn Sci 10:424–430
Owen AM, McMillan KM, Laird AR, Bullmore E (2005) N-back working memory paradigm: a meta-analysis of normative functional neuroimaging studies. Hum Brain Mapp 25:46–59
Phillips WA, Christie DFM (1977) Components of visual memory. Q J Exp Psychol 29:117–133
Postle BR (2006) Working memory as an emergent property of the mind and brain. Neuroscience 139:23–38
Postle BR, Berger JS, Taich AM, D’Esposito M (2000) Activity in human frontal cortex associated with spatial working memory and saccadic behavior. J Cogn Neurosci 12(Suppl 2):2–14
Postle BR, Druzgal TJ, D’Esposito M (2003) Seeking the neural substrates of visual working memory storage. Cortex J Devoted Study Nerv Syst Behav 39:927–946
Puce A, Allison T, Gore JC, McCarthy G (1995) Face-sensitive regions in human extrastriate cortex studied by functional MRI. J Neurophysiol 74:1192–1199
Ranganath C, DeGutis J, D’Esposito M (2004a) Category-specific modulation of inferior temporal activity during working memory encoding and maintenance. Brain Res Cogn Brain Res 20:37–45
Ranganath C, Cohen MX, Dam C, D’Esposito M (2004b) Inferior temporal, prefrontal, and hippocampal contributions to visual working memory maintenance and associative memory retrieval. J Neurosci Official J Soc Neurosci 24:3917–3925
Riggall AC, Postle BR (2012) The relationship between working memory storage and elevated activity as measured with functional magnetic resonance imaging. J Neurosci Official J Soc Neurosci 32:12990–12998
Rottschy C, Langner R, Dogan I, Reetz K, Laird AR, Schulz JB, Fox PT, Eickhoff SB (2012) Modelling neural correlates of working memory: a coordinate-based meta-analysis. Neuroimage 60:830–846
Serences JT, Ester EF, Vogel EK, Awh E (2009) Stimulus-specific delay activity in human primary visual cortex. Psychol Sci 20:207–214
Sreenivasan KK, Vytlacil J, D’Esposito M (2014) Distributed and dynamic storage of working memory stimulus information in extrastriate cortex. J Cogn Neurosci 26:1141–1153
Stokes MG, Kusunoki M, Sigala N, Nili H, Gaffan D, Duncan J (2013) Dynamic coding for cognitive control in prefrontal cortex. Neuron 78:364–375
Sugase-Miyamoto Y, Liu Z, Wiener MC, Optican LM, Richmond BJ (2008) Short-term memory trace in rapidly adapting synapses of inferior temporal cortex. PLoS Comp Biol 4:e1000073
Super H, Spekreijse H, Lamme VA (2001) A neural correlate of working memory in the monkey primary visual cortex. Science 293:120–124
Tamber-Rosenau BJ, Esterman M, Chiu YC, Yantis S (2011) Cortical mechanisms of cognitive control for shifting attention in vision and working memory. J Cogn Neurosci 23:2905–2919
Todd MT, Nystrom LE, Cohen JD (2013) Confounds in multivariate pattern analysis: theory and rule representation case study. Neuroimage 77:157–165
van den Berg R, Awh E, Ma WJ (2014) Factorial comparison of working memory models. Psychol Rev 121:124–149
Wager TD, Smith EE (2003) Neuroimaging studies of working memory: a meta-analysis. Cogn Affect Behav Neurosci 3:255–274
Wilken P, Ma WJ (2004) A detection theory account of change detection. J Vis 4:1120–1135
Yoon JH, Curtis CE, D’Esposito M (2006) Differential effects of distraction during working memory on delay-period activity in the prefrontal cortex and the visual association cortex. Neuroimage 29:1117–1126
Zhang W, Luck SJ (2008) Discrete fixed-resolution representations in visual working memory. Nature 453:233–235
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Nee, D.E., D’Esposito, M. (2016). The Representational Basis of Working Memory. In: Clark, R.E., Martin, S. (eds) Behavioral Neuroscience of Learning and Memory. Current Topics in Behavioral Neurosciences, vol 37. Springer, Cham. https://doi.org/10.1007/7854_2016_456
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DOI: https://doi.org/10.1007/7854_2016_456
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