From cognitive to neural models of working memory

Working memory refers to the temporary retention of information that was just experienced or just retrieved from long-term memory but no longer exists in the external environment. These internal representations are short-lived, but can be stored for longer periods of time through active maintenance or rehearsal strategies, and can be subjected to various operations that manipulate the information in such a way that makes it useful for goal-directed behaviour. Empirical studies of working memory using neuroscientific techniques, such as neuronal recordings in monkeys or functional neuroimaging in humans, have advanced our knowledge of the underlying neural mechanisms of working memory. This rich dataset can be reconciled with behavioural findings derived from investigating the cognitive mechanisms underlying working memory. In this paper, I review the progress that has been made towards this effort by illustrating how investigations of the neural mechanisms underlying working memory can be influenced by cognitive models and, in turn, how cognitive models can be shaped and modified by neuroscientific data. One conclusion that arises from this research is that working memory can be viewed as neither a unitary nor a dedicated system. A network of brain regions, including the prefrontal cortex (PFC), is critical for the active maintenance of internal representations that are necessary for goal-directed behaviour. Thus, working memory is not localized to a single brain region but probably is an emergent property of the functional interactions between the PFC and the rest of the brain.

[1]  Edward E. Smith,et al.  Rehearsal in Spatial Working Memory: Evidence From Neuroimaging , 1999 .

[2]  P. Goldman-Rakic,et al.  Dorsolateral prefrontal lesions and oculomotor delayed-response performance: evidence for mnemonic "scotomas" , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  M Gangitano,et al.  Segregation of areas related to visual working memory in the prefrontal cortex revealed by rTMS. , 2002, Cerebral cortex.

[4]  D. J. Murray Articulation and acoustic confusability in short-term memory. , 1968 .

[5]  K J Friston,et al.  The predictive value of changes in effective connectivity for human learning. , 1999, Science.

[6]  Donald A. Norman,et al.  Attention to Action , 1986 .

[7]  K. Nakamura,et al.  Mnemonic firing of neurons in the monkey temporal pole during a visual recognition memory task. , 1995, Journal of neurophysiology.

[8]  R. Passingham,et al.  Changes of cortico-striatal effective connectivity during visuomotor learning. , 2002, Cerebral cortex.

[9]  A. Baddeley The episodic buffer: a new component of working memory? , 2000, Trends in Cognitive Sciences.

[10]  J. Fuster Memory in the cerebral cortex , 1994 .

[11]  Anthony Randal McIntosh,et al.  Towards a network theory of cognition , 2000, Neural Networks.

[12]  T. Sejnowski,et al.  Neurocomputational models of working memory , 2000, Nature Neuroscience.

[13]  P. Goldman-Rakic,et al.  Coding Specificity in Cortical Microcircuits: A Multiple-Electrode Analysis of Primate Prefrontal Cortex , 2001, The Journal of Neuroscience.

[14]  Karalyn Patterson,et al.  The reign of typicality in semantic memory , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[15]  T. Allison,et al.  Electrophysiological Studies of Face Perception in Humans , 1996, Journal of Cognitive Neuroscience.

[16]  Michael X. Cohen,et al.  Inferior Temporal, Prefrontal, and Hippocampal Contributions to Visual Working Memory Maintenance and Associative Memory Retrieval , 2004, The Journal of Neuroscience.

[17]  Karl J. Friston,et al.  Attentional modulation of effective connectivity from V2 to V5/MT in humans. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[18]  G. Hickok,et al.  Auditory–Motor Interaction Revealed by fMRI: Speech, Music, and Working Memory in Area Spt , 2003 .

[19]  Patricia S. Goldman TOPOGRAPHY OF COGNITION: Parallel Distributed Networks in Primate Association Cortex , 1988 .

[20]  E. Maguire,et al.  Patterns of hippocampal‐cortical interaction dissociate temporal lobe memory subsystems , 2000, Hippocampus.

[21]  J. Driver,et al.  Modulation of visual processing by attention and emotion: windows on causal interactions between human brain regions , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[22]  N. Cowan An embedded-processes model of working memory , 1999 .

[23]  R. Knight,et al.  Prefrontal cortex regulates inhibition and excitation in distributed neural networks. , 1999, Acta psychologica.

[24]  J. Fuster Cortex and Mind , 2002 .

[25]  J B Poline,et al.  Transient Activity in the Human Calcarine Cortex During Visual-Mental Imagery: An Event-Related fMRI Study , 2000, Journal of Cognitive Neuroscience.

[26]  B. Postle,et al.  Effects of verbal and nonverbal interference on spatial and object visual working memory , 2005, Memory & cognition.

[27]  A. Baddeley,et al.  The multi-component model of working memory: Explorations in experimental cognitive psychology , 2006, Neuroscience.

[28]  Jordan Grafman,et al.  Handbook of Neuropsychology , 1991 .

[29]  Jonathan D. Cohen,et al.  Prefrontal cortex and dynamic categorization tasks: representational organization and neuromodulatory control. , 2002, Cerebral cortex.

[30]  T. Robbins Shifting and stopping: fronto-striatal substrates, neurochemical modulation and clinical implications , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[31]  Richard S. J. Frackowiak,et al.  The neural correlates of the verbal component of working memory , 1993, Nature.

[32]  Mark D'Esposito,et al.  A functional MRI study of the effects of bromocriptine, a dopamine receptor agonist, on component processes of working memory , 2005, Psychopharmacology.

[33]  J. Fuster The Prefrontal Cortex , 1997 .

[34]  J. Fuster,et al.  Delayed-matching and delayed-response deficit from cooling dorsolateral prefrontal cortex in monkeys. , 1976, Journal of comparative and physiological psychology.

[35]  Adam Gazzaley,et al.  Measuring functional connectivity during distinct stages of a cognitive task , 2004, NeuroImage.

[36]  T. Sawaguchi,et al.  The effects of dopamine and its antagonists on directional delay-period activity of prefrontal neurons in monkeys during an oculomotor delayed-response task , 2001, Neuroscience Research.

[37]  G. E. Alexander,et al.  Neuron Activity Related to Short-Term Memory , 1971, Science.

[38]  T. Allison,et al.  Word recognition in the human inferior temporal lobe , 1994, Nature.

[39]  Karl J. Friston,et al.  Functional Connectivity: The Principal-Component Analysis of Large (PET) Data Sets , 1993, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[40]  C. Curtis,et al.  Persistent activity in the prefrontal cortex during working memory , 2003, Trends in Cognitive Sciences.

[41]  H. Niki,et al.  Prefrontal cortical unit activity and delayed alternation performance in monkeys. , 1971, Journal of neurophysiology.

[42]  J. Grafman,et al.  Human prefrontal cortex: processing and representational perspectives , 2003, Nature Reviews Neuroscience.

[43]  Clayton E. Curtis,et al.  Differential effects of distraction during working memory on delay-period activity in the prefrontal cortex and the visual association cortex , 2006, NeuroImage.

[44]  J. Fuster Prefrontal Cortex , 2018 .

[45]  T. Sejnowski,et al.  Dopamine-mediated stabilization of delay-period activity in a network model of prefrontal cortex. , 2000, Journal of neurophysiology.

[46]  Hsuan-Chih Chen,et al.  Brain Responses to Segmentally and Tonally Induced Semantic Violations in Cantonese , 2005, Journal of Cognitive Neuroscience.

[47]  Elso Arruda,et al.  The prefrontal cortex: anatomy, physiology and neuropsychology of the frontal lobo , 1990 .

[48]  David J. M. Kraemer,et al.  Musical imagery: Sound of silence activates auditory cortex , 2005, Nature.

[49]  D. Norman,et al.  Attention to Action: Willed and Automatic Control of Behavior Technical Report No. 8006. , 1980 .

[50]  P. Goldman-Rakic,et al.  Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. , 1989, Journal of neurophysiology.

[51]  Leslie G. Ungerleider,et al.  An area specialized for spatial working memory in human frontal cortex. , 1998, Science.

[52]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[53]  Iroise Dumontheil,et al.  Function and localization within rostral prefrontal cortex (area 10) , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[54]  E. Bullmore,et al.  Activation of auditory cortex during silent lipreading. , 1997, Science.

[55]  T. Robbins,et al.  Chemistry of the adaptive mind , 2004, Philosophical Transactions of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences.

[56]  Tim Shallice,et al.  Neuropsychological impairments of short-term memory , 1992 .

[57]  Shane T. Mueller,et al.  Models of Working Memory: Insights into Working Memory from the Perspective of the EPIC Architecture for Modeling Skilled Perceptual-Motor and Cognitive Human Performance , 1998 .

[58]  Richard J. Brown Neuropsychology Mental Structure , 1989 .

[59]  Y. Miyashita,et al.  Top-down signal from prefrontal cortex in executive control of memory retrieval , 1999, Nature.

[60]  R. Knight,et al.  Contribution of Human Prefrontal Cortex to Delay Performance , 1998, Journal of Cognitive Neuroscience.

[61]  B. Postle,et al.  Prefrontal cortical contributions to working memory: evidence from event-related fMRI studies , 2000, Experimental Brain Research.

[62]  Jonathan D. Cohen,et al.  Computational perspectives on dopamine function in prefrontal cortex , 2002, Current Opinion in Neurobiology.

[63]  O. Bertrand,et al.  Oscillatory Synchrony between Human Extrastriate Areas during Visual Short-Term Memory Maintenance , 2001, The Journal of Neuroscience.

[64]  Edward E. Smith,et al.  Dissociation of Storage and Rehearsal in Verbal Working Memory: Evidence From Positron Emission Tomography , 1996 .

[65]  M. Petrides Lateral prefrontal cortex: architectonic and functional organization , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[66]  M. D’Esposito,et al.  Medial Temporal Lobe Activity Associated with Active Maintenance of Novel Information , 2001, Neuron.

[67]  Karl J. Friston,et al.  Investigations of the functional anatomy of attention using the stroop test , 1993, Neuropsychologia.

[68]  Karl J. Friston,et al.  Attention to Action: Specific Modulation of Corticocortical Interactions in Humans , 2001, NeuroImage.

[69]  Thomas E. Hazy,et al.  Banishing the homunculus: Making working memory work , 2006, Neuroscience.

[70]  M. D’Esposito,et al.  Functional connectivity during working memory maintenance , 2004, Cognitive, affective & behavioral neuroscience.

[71]  D. Stuss,et al.  Is there a dysexecutive syndrome? , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[72]  P. Goldman-Rakic,et al.  Matching patterns of activity in primate prefrontal area 8a and parietal area 7ip neurons during a spatial working memory task. , 1998, Journal of neurophysiology.

[73]  James L. McClelland,et al.  On the control of automatic processes: a parallel distributed processing account of the Stroop effect. , 1990, Psychological review.

[74]  M. D’Esposito Working memory. , 2008, Handbook of clinical neurology.

[75]  Jonathan D. Cohen,et al.  A Biologically Based Computational Model of Working Memory , 1999 .

[76]  A. McIntosh,et al.  Understanding Neural Interactions in Learning and Memory Using Functional Neuroimaging , 1998, Annals of the New York Academy of Sciences.

[77]  Y. Miyashita,et al.  Neuronal correlate of pictorial short-term memory in the primate temporal cortexYasushi Miyashita , 1988, Nature.

[78]  C. Fiebach,et al.  Modulation of Inferotemporal Cortex Activation during Verbal Working Memory Maintenance , 2006, Neuron.

[79]  Bradley R. Postle,et al.  Delay-period Activity in the Prefrontal Cortex: One Function Is Sensory Gating , 2005, Journal of Cognitive Neuroscience.

[80]  R. Berndt,et al.  Working memory retention systems: a state of activated long-term memory. , 2003, The Behavioral and brain sciences.

[81]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

[82]  J. Fuster,et al.  Functional interactions between inferotemporal and prefrontal cortex in a cognitive task , 1985, Brain Research.

[83]  R. E. Passingham,et al.  Cerebral cortex, vol. 4, association and auditory cortices A. Peters andE. G. Jones (eds). Plenum Press, New York (1985). 359 pp. £52.25 , 1987, Neuroscience.

[84]  Daniel Y. Kimberg,et al.  Cognitive Functions in the Prefrontal Cortex—Working Memory and Executive Control , 1997 .

[85]  J. Jonides,et al.  Overlapping mechanisms of attention and spatial working memory , 2001, Trends in Cognitive Sciences.

[86]  Jeffrey W. Cooney,et al.  Is the Prefrontal Cortex Necessary for Delay Task Performance? Evidence from Lesion and fMRI Data , 2006, Journal of the International Neuropsychological Society.

[87]  R. Desimone,et al.  Activity of neurons in anterior inferior temporal cortex during a short- term memory task , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[88]  Mark D'Esposito,et al.  Searching for “the Top” in Top-Down Control , 2005, Neuron.

[89]  Clayton E. Curtis,et al.  Maintenance of Spatial and Motor Codes during Oculomotor Delayed Response Tasks , 2004, The Journal of Neuroscience.

[90]  Noam Sobel,et al.  Attentional modulation in human primary olfactory cortex , 2005, Nature Neuroscience.

[91]  Robert T. Knight,et al.  Top-down Enhancement and Suppression of the Magnitude and Speed of Neural Activity , 2005, Journal of Cognitive Neuroscience.

[92]  N. Cowan Evolving conceptions of memory storage, selective attention, and their mutual constraints within the human information-processing system. , 1988, Psychological bulletin.

[93]  J. Fuster Cortical dynamics of memory. , 1998, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[94]  R. Logie Visuo-spatial Working Memory , 1994 .

[95]  David J Heeger,et al.  Neural correlates of sustained spatial attention in human early visual cortex. , 2007, Journal of neurophysiology.

[96]  Lorraine K Tyler,et al.  Morphology, language and the brain: the decompositional substrate for language comprehension , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[97]  M. D’Esposito,et al.  Dissecting Contributions of Prefrontal Cortex and Fusiform Face Area to Face Working Memory , 2003, Journal of Cognitive Neuroscience.

[98]  W. Singer,et al.  Dynamic predictions: Oscillations and synchrony in top–down processing , 2001, Nature Reviews Neuroscience.

[99]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[100]  S. Funahashi,et al.  Neuronal interactions related to working memory processes in the primate prefrontal cortex revealed by cross-correlation analysis. , 2000, Cerebral cortex.

[101]  Stanislas Dehaene,et al.  Specialization within the ventral stream: the case for the visual word form area , 2004, NeuroImage.

[102]  Xiao-Jing Wang Synaptic reverberation underlying mnemonic persistent activity , 2001, Trends in Neurosciences.