Neural mechanisms of order information processing in working memory
AbstractThe ability to encode and maintain the exact order of short sequences of stimuli or events is often crucial to our ability for effective high-order planning. However, it is not yet clear which neural mechanisms underpin this process. Several studies suggest that in comparison with item recognition temporal order coding activates prefrontal and parietal brain regions. Results of various studies tend to favour the hypothesis that the order of the stimuli is represented and encoded on several stages, from primacy and recency estimates to the exact position of the item in a sequence. Different brain regions play a different role in this process. Dorsolateral prefrontal cortex has a more general role in attention, while the premotor cortex is more involved in the process of information grouping. Parietal lobe and hippocampus also play a significant role in order processing as they enable the representation of distance. Moreover, order maintenance is associated with the existence of neural oscillators that operate at different frequencies. Electrophysiological studies revealed that theta and alpha oscillations play an important role in the maintenance of temporal order information. Those EEG oscillations are differentially associated with processes that support the maintenance of order information and item recognition. Various studies suggest a link between prefrontal areas and memory for temporal order, implying that EEG neural oscillations in the prefrontal cortex may play a role in the maintenance of information on temporal order.
Eysenck MW, Keane MT. Cognitive Psychology: A Student’s Handbook.5th edition. East Sussex: Psychology Press; 2005.
Baddeley A. Working memory: looking back and looking forward. Nat Rev Neurosci 2003; 4: 829–39.
Smith EE, Jonides J. Storage and executive processes in the frontal lobes. Science 1999; 283: 1657–61.
Alvarez P, Zola-Morgan S, Squire LR. The animal model of human amnesia: long-term memory impaired and short-term memory intact. Proc Natl Acad Sci U S A 1994; 91: 5637–41.
Scoville WB, Milner B. Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 1957; 20: 11–21.
Jonides J, Reuter-Lorenz PA, Smith EE, Awh E, Barnes LL, Drain M et al. Verbal and spatial working memory in humans. In: Medin D, ed. The Psychology of Learning and Memory. New York: Academic Press; 1996. p. 165–92.
Miller EK, Cohen JD. An integrative theory of prefrontal cortex function. Annu Rev Neurosci 2001; 24: 167–202.
Cabeza R, Mangels J, Nyberg L, Habib R, Houle S, McIntosh AR, et al. Brain regions differentially involved in remembering what and when: a PET study. Neuron 1997; 19: 863–70.
Milner B, Petrides M, Smith ML. Frontal lobes and the temporal organization of memory. Hum Neurobiol 1985; 4: 137–42.
Kesner RP, Hopkins RO, Fineman B. Item and order dissociation in humans with prefrontal cortex damage. Neuropsychologia 1994; 32: 881–91.
Mangels JA. Strategic processing and memory for temporal order in patients with frontal lobe lesions. Neuropsychology 1997; 11: 207–21.
McAndrews MP, Milner B. The frontal cortex and memory for temporal order. Neuropsychologia
; 29: 849–59.
Milner B, Corsi P, Leonard G. Frontal-lobe contribution to recency judgements. Neuropsychologia
; 29: 601–18.
Petrides M. Functional specialization within the dorsolateral frontal cortex for serial order memory. Proc R Soc Lond B Biol Sci 1991; 246: 299–306.
Milner B. Interhemispheric differences in the localization of psychological processes in man. Br Med Bull 1971; 27: 272–7.
Marshuetz C, Smith EE. Working memory for order information: multiple cognitive and neural mechanisms. Neuroscience 2006; 139: 195–200.
Suzuki M, Fujii T, Tsukiura T, Okuda J, Umetsu A, Nagasaka T, et al. Neural basis of temporal context memory: a functional MRI study. NeuroImage 2002; 17: 1790–6.
Marshuetz C, Smith EE, Jonides J, DeGutis J, Chenevert TL. Order information in working memory: fMRI evidence for parietal and prefrontal mechanisms. J Cogn Neurosc 2000; 12: 130–44.
Amiez C, Petrides M. Selective involvement of the mid-dorsolateral prefrontal cortex in the coding of the serial order of visual stimuli in working memory. Proc Natl Acad Sci U S A 2007; 104: 13786–91.
Marshuetz C. Order information in working memory: an integrative review of evidence from brain and behavior. Psychol Bull 2005; 131: 323–39.
Sakai K, Passingham RE. Prefrontal interactions reflect future task operations. Nat Neurosci 2003; 6: 75–81.
Marshuetz C, Reuter-Lorenz PA, Smith EE, Jonides J, Noll DC. Working memory for order and the parietal cortex: an event-related functional magnetic resonance imaging study. Neuroscience 2006; 139: 311–6.
Moyer RS, Landauer TK. Time required for judgements of numerical inequality. Nature 1967; 215: 1519–20.
Burgess N, Hitch GJ. Memory for serial order: A network model of the phonological loop and its timing. Psychol Rev 1999; 106: 551–81.
Lee C, Estes WK. Item and order information in short-term memory: evidence for multilevel perturbation processes. J Exp Psychol Hum Learn Mem 1981; 7: 149–69.
Miller GA. The magical number seven plus or minus two: some limits on our capacity for processing information. Psychol Rev 1956; 63: 81–97.
Henson RN, Burgess N, Frith CD. Recoding, storage, rehearsal and grouping in verbal short-term
memory: an fMRI study. Neuropsychologia 2000; 38: 426–40.
Zhang DR, Li ZH, Chen XC, Wang ZX, Zhang XC, Xiao MM, et al. Functional comparison of primacy, middle and recency retrieval in human auditory short-term memory: an event-related fMRI study. Brain Res Cogn Brain Res 2003; 16: 91–8.
Hopkins RO, Kesner RP, Goldstein M. Item and order recognition memory in subjects with hypoxic brain injury. Brain Cogn 1995; 27: 180–201.
Mayes AR, Isaac CL, Holdstock JS, Hunkin NM, Montaldi D, Downes JJ, et al. Memory for single items, word pairs, and temporal order of different kinds in a patient with selective hippocampal lesions. Cogn Neuropsychol 2001; 18: 97–123.
Kesner RP, Hopkins RO. Short-term memory for duration and distance in humans: role of the hippocampus. Neuropsychology 2001; 15: 58–68.
Fortin NJ, Agster KL, Eichenbaum HB. Critical role of the hippocampus in memory for sequences of events. Nat Neurosci 2002; 5: 458–62.
Carpenter AF, Georgopoulos AP, Pellizzer G. Motor cortical encoding of serial order in a context--recall task. Science 1999; 283: 1752–7.
Huxter J, Burgess N, O’Keefe J. Independent rate and temporal coding in hippocampal pyramidal cells. Nature 2003; 425: 828–32.
Konishi S, Uchida I, Okuaki T, Machida T, Shirouzu I, Miyashita Y. Neural correlates of recency judgment. J Neurosci 2002; 22: 9549–55.
Cabeza R, Anderson ND, Houle S, Mangels JA, Nyberg L. Age-related differences in neural activity during item and temporal-order memory retrieval: a positron emission tomography study. J Cogn Neurosci 2000; 12: 197–206.
Harrington DL, Haaland KY, Knight RT. Cortical networks underlying mechanisms of time perception. J Neurosci 1998; 18: 1085–95.
Pinel P, Dehaene S, Riviere D, LeBihan D. Modulation of parietal activation by semantic distance in a number comparison task. Neuroimage 2001; 14: 1013–26.
Pinel P, Piazza M, Le Bihan D, Dehaene S. Distributed and overlapping cerebral representations of number, size, and luminance during comparative judgments. Neuron 2004; 41: 983–93.
Cohen L, Dehaene S. Cerebral networks for number processing: Evidence from a case of posterior callosal lesion. Neurocase 1996; 2: 155–74.
Fias W, Lammertyn J, Reynvoet B, Dupont P, Orban GA. Parietal representation of symbolic and nonsymbolic magnitude. J Cogn Neurosci 2003; 15: 47–56.
Jensen O. Maintenance of multiple working memory items by temporal segmentation. Neuroscience 2006; 139: 237–49.
Lisman JE, Idiart MA. Storage of 7 +/- 2 short--term memories in oscillatory subcycles. Science 1995; 267: 1512–5.
Jokisch D, Jensen O. Modulation of gamma and alpha activity during a working memory task engaging the dorsal or ventral stream. J Neurosci 2007; 27: 3244–51.
Botvinick MM, Plaut DC. Short-term memory for serial order: a recurrent neural network model. Psychol Rev 2006; 113: 201–33.
Ninokura Y, Mushiake H, Tanji J. Representation of the temporal order of visual objects in the primate lateral prefrontal cortex. J Neurophysiol 2003; 89: 2868–73.
Jensen O, Lisman JE. An oscillatory short-term memory buffer model can account for data on the Sternberg task. J Neurosci 1998; 18: 10688–99.
Gundel A, Wilson GF. Topographical changes in the ongoing EEG related to the difficulty of mental tasks. Brain Topogr 1992; 5: 17–25.
Iramina K, Ueno S, Matsuoka S. MEG and EEG topography of frontal midline theta rhythm and source localization. Brain Topogr 1996; 8: 329–31.
Krause CM, Lang AH, Laine M, Kuusisto M, Porn B. Event-related EEG desynchronization and synchronization during an auditory memory task. Electroencephalogr Clin Neurophysiol 1996; 98: 319–26.
Tallon-Baudry C, Bertrand O, Delpuech C, Permier J. Oscillatory gamma-band (30–70 Hz) activity induced by a visual search task in humans. J Neurosci 1997; 17: 722–34.
Tallon-Baudry C, Bertrand O, Peronnet F, Pernier J. Induced gamma-band activity during the delay of a visual short-term memory task in humans. J Neurosci 1998; 18: 4244–54.
Gevins A, Smith ME, McEvoy L, Yu D. High-resolution EEG mapping of cortical activation related to working memory: effects of task difficulty, type of processing, and practice. Cereb Cortex 1997; 7: 374–85.
Jensen O, Tesche CD. Frontal theta activity in humans increases with memory load in a working memory task. Eur J Neurosci 2002; 15: 1395–9.
Meltzer JA, Zaveri HP, Goncharova II, Distasio MM, Papademetris X, Spencer SS, et al. Effects of working memory load on oscillatory power in human intracranial EEG. Cereb Cortex 2008; 18: 1843–55.
Jensen O, Gelfand J, Kounios J, Lisman JE. Oscillations in the alpha band (9–12 Hz) increase with memory load during retention in a short-term memory task. Cereb Cortex 2002; 12: 877–82.
Sauseng P, Klimesch W, Heise KF, Gruber WR, Holz E, Karim AA, et al. Brain oscillatory substrates of visual short-term memory capacity. Curr Biol 2009; 19: 1846–52.
Scheeringa R, Petersson KM, Oostenveld R, Norris DG, Hagoort P, Bastiaansen MC. Trial-by-trial coupling between EEG and BOLD identifies networks related to alpha and theta EEG power increases during working memory maintenance. Neuroimage 2009; 44: 1224–38.
Hasher L, Zacks RT. Automatic and effortful processes in memory. J Exp Psychol Gen 1979; 108: 356–88.
Hsieh LT, Ekstrom AD, Ranganath C. Neural oscillations associated with item and temporal order maintenance in working memory. J Neurosci 2011; 31: 10803–10.
Tsujimoto T, Shimazu H, Isomura Y. Direct recording of theta oscillations in primate prefrontal and anterior cingulate cortices. J Neurophysiol 2006; 95: 2987–3000.
Buzsaki G. Theta oscillations in the hippocampus. Neuron 2002; 33: 325–40.
Ekstrom A, Viskontas I, Kahana M, Jacobs J, Upchurch K, Bookheimer S, et al. Contrasting roles of neural firing rate and local field potentials in human memory. Hippocampus 2007; 17: 606–17.
Benchenane K, Peyrache A, Khamassi M, Tiemey PL, Gioanni Y, Battaglia FP, et al. Coherent theta oscillations and reorganization of spike timing in the hippocampal- prefrontal network upon learning. Neuron 2010; 66: 921–36.
Hyman JM, Zilli EA, Paley AM, Hasselmo ME. Medial prefrontal cortex cells show dynamic modulation with the hippocampal theta rhythm dependent on behavior. Hippocampus 2005; 15: 739–49.
O’Reilly RC, McClelland JL. Hippocampal conjunctive encoding, storage, and recall: avoiding a trade-off. Hippocampus 1994; 4: 661–82.
Jay TM, Glowinski J, Thierry AM. Selectivity of the hippocampal projection to the prelimbic area of the prefrontal cortex in the rat. Brain Res 1989; 505: 337–40.
Anderson KL, Rajagovindan R, Ghacibeh GA, Meador KJ, Ding M. Theta oscillations mediate interaction between prefrontal cortex and medial temporal lobe in human memory. Cereb Cortex 2010; 20: 1604–12.
Kesner RP, Holbrook T. Dissociation of item and order spatial memory in rats following medial prefrontal cortex lesions. Neuropsychologia 1987; 25: 653–64.
Li SC, Lewandowsky S. Forward and backward recall: Different retrieval processes. J Exp Psychol: Learning, Memory, and Cognition 1995; 21: 837–47.