The functional neuroanatomy of multitasking: Combining dual tasking with a short term memory task

Insight into the neural architecture of multitasking is crucial when investigating the pathophysiology of multitasking deficits in clinical populations. Presently, little is known about how the brain combines dual-tasking with a concurrent short-term memory task, despite the relevance of this mental operation in daily life and the frequency of complaints related to this process, in disease. In this study we aimed to examine how the brain responds when a memory task is added to dual-tasking. Thirty-three right-handed healthy volunteers (20 females, mean age 39.9 ± 5.8) were examined with functional brain imaging (fMRI). The paradigm consisted of two cross-modal single tasks (a visual and auditory temporal same-different task with short delay), a dual-task combining both single tasks simultaneously and a multi-task condition, combining the dual-task with an additional short-term memory task (temporal same-different visual task with long delay). Dual-tasking compared to both individual visual and auditory single tasks activated a predominantly right-sided fronto-parietal network and the cerebellum. When adding the additional short-term memory task, a larger and more bilateral frontoparietal network was recruited. We found enhanced activity during multitasking in components of the network that were already involved in dual-tasking, suggesting increased working memory demands, as well as recruitment of multitask-specific components including areas that are likely to be involved in online holding of visual stimuli in short-term memory such as occipito-temporal cortex. These results confirm concurrent neural processing of a visual short-term memory task during dual-tasking and provide evidence for an effective fMRI multitasking paradigm.

[1]  J. O’Shaughnessy,et al.  Chemotherapy-related cognitive dysfunction in breast cancer. , 2003, Seminars in oncology nursing.

[2]  Patrick Dupont,et al.  Lesion evidence for the critical role of the intraparietal sulcus in spatial attention. , 2011, Brain : a journal of neurology.

[3]  Jan Gläscher,et al.  Visualization of Group Inference Data in Functional Neuroimaging , 2009, Neuroinformatics.

[4]  C. Summerfield,et al.  Two Mechanisms for Task Switching in the Prefrontal Cortex , 2009, The Journal of Neuroscience.

[5]  Hauke R. Heekeren,et al.  Performance level modulates adult age differences in brain activation during spatial working memory , 2009, Proceedings of the National Academy of Sciences.

[6]  J. Pernier,et al.  Induced gamma-band activity during the delay of a visual short-term memory task in humans. , 1998, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  Yuhong Jiang,et al.  Visual working memory for simple and complex features: An fMRI study , 2006, NeuroImage.

[8]  A. Leemans,et al.  Longitudinal assessment of chemotherapy-induced structural changes in cerebral white matter and its correlation with impaired cognitive functioning. , 2012, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[9]  H. Pashler Dual-task interference in simple tasks: data and theory. , 1994, Psychological bulletin.

[10]  A. Dove,et al.  Prefrontal cortex activation in task switching: an event-related fMRI study. , 2000, Brain research. Cognitive brain research.

[11]  A. Baddeley,et al.  Dual-task performance in dysexecutive and nondysexecutive patients with a frontal lesion. , 1997, Neuropsychology.

[12]  S. Fortin,et al.  Strategic Sequence Planning and Prospective Memory Impairments in Frontally Lesioned Head Trauma Patients Performing Activities of Daily Living , 2002, Brain and Cognition.

[13]  E. Macaluso,et al.  The contribution of working memory to divided attention , 2013, Human brain mapping.

[14]  P W Burgess,et al.  Strategy application disorder: the role of the frontal lobes in human multitasking , 2000, Psychological research.

[15]  Yaakov Stern,et al.  Task difficulty modulates young–old differences in network expression , 2012, Brain Research.

[16]  W Cahn,et al.  Excessive recruitment of neural systems subserving logical reasoning in schizophrenia. , 2002, Brain : a journal of neurology.

[17]  M. Mesulam Principles of Behavioral and Cognitive Neurology , 2000 .

[18]  David C. Van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex , 2005, NeuroImage.

[19]  M. Mesulam,et al.  Principles of behavioral and cognitive neurology, 2nd ed. , 2000 .

[20]  R. D. Gordon,et al.  Executive control of visual attention in dual-task situations. , 2001, Psychological review.

[21]  John J. Rieser,et al.  Blindness and Brain Plasticity in Navigation and Object Perception , 2007 .

[22]  M. Sigman,et al.  Brain Mechanisms of Serial and Parallel Processing during Dual-Task Performance , 2008, The Journal of Neuroscience.

[23]  J. Aggleton,et al.  The functional anatomy of visual-tactile integration in man: a study using positron emission tomography , 2000, Neuropsychologia.

[24]  Alexander Leemans,et al.  Chemotherapy‐induced structural changes in cerebral white matter and its correlation with impaired cognitive functioning in breast cancer patients , 2011, Human brain mapping.

[25]  M. Farah The neural basis of mental imagery , 1989, Trends in Neurosciences.

[26]  Helen Barbas,et al.  Anterior Cingulate Synapses in Prefrontal Areas 10 and 46 Suggest Differential Influence in Cognitive Control , 2010, The Journal of Neuroscience.

[27]  Selective deficit of divided attention following traumatic brain injury: case reports. , 2012, The Tokai journal of experimental and clinical medicine.

[28]  A. Scholey,et al.  The effects of multitasking on psychological stress reactivity in recreational users of cannabis and MDMA , 2012, Human psychopharmacology.

[29]  Robert J. Zatorre,et al.  Neural substrates for dividing and focusing attention between simultaneous auditory and visual events , 2006, NeuroImage.

[30]  Christopher L. Asplund,et al.  Isolation of a Central Bottleneck of Information Processing with Time-Resolved fMRI , 2006, Neuron.

[31]  A. Treisman,et al.  Attentional demands predict short-term memory load response in posterior parietal cortex , 2009, Neuropsychologia.

[32]  René Marois,et al.  Working Memory Encoding Delays Top–Down Attention to Visual Cortex , 2011, Journal of Cognitive Neuroscience.

[33]  G. Kwakkel,et al.  Attending to the task: interference effects of functional tasks on walking in Parkinson's disease and the roles of cognition, depression, fatigue, and balance. , 2004, Archives of physical medicine and rehabilitation.

[34]  M. Petrides The role of the mid-dorsolateral prefrontal cortex in working memory , 2000, Experimental Brain Research.

[35]  Catherine Tallon-Baudry,et al.  Induced γ-Band Activity during the Delay of a Visual Short-Term Memory Task in Humans , 1998, The Journal of Neuroscience.

[36]  Rainer Goebel,et al.  Integration of “what” and “where” in frontal cortex during visual imagery of scenes , 2012, NeuroImage.

[37]  Torsten Schubert,et al.  Task-order coordination in dual-task performance and the lateral prefrontal cortex: an event-related fMRI study , 2006, Psychological research.

[38]  H. Diener,et al.  On the neural basis of focused and divided attention. , 2005, Brain research. Cognitive brain research.

[39]  Christian Kaufmann,et al.  Human prefrontal and sensory cortical activity during divided attention tasks , 2003, Human brain mapping.

[40]  Patrick Dupont,et al.  The associative-semantic network for words and pictures: Effective connectivity and graph analysis , 2013, Brain and Language.

[41]  Y. Miyashita,et al.  No‐go dominant brain activity in human inferior prefrontal cortex revealed by functional magnetic resonance imaging , 1998, The European journal of neuroscience.

[42]  B. Collins,et al.  Clearing the Air: A Review of Our Current Understanding of “Chemo Fog” , 2013, Current Oncology Reports.

[43]  Joseph A Maldjian,et al.  Cross‐modal sensory processing in the anterior cingulate and medial prefrontal cortices , 2003, Human brain mapping.

[44]  Ronald R. Peeters,et al.  Attentional priorities and access to short-term memory: Parietal interactions , 2012, NeuroImage.

[45]  S. Frisch,et al.  The interleaving of actions in everyday life multitasking demands. , 2012, Journal of neuropsychology.

[46]  Takao Suzuki,et al.  Relationship between dual‐task performance and neurocognitive measures in older adults with mild cognitive impairment , 2013, Geriatrics & gerontology international.

[47]  M. D’Esposito,et al.  The neural effect of stimulus-response modality compatibility on dual-task performance: an fMRI study , 2006, Psychological research.

[48]  M. Posner,et al.  Attention, self-regulation and consciousness. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[49]  Eric Ruthruff,et al.  How strategic is the central bottleneck: can it be overcome by trying harder? , 2009, Journal of experimental psychology. Human perception and performance.

[50]  Kaustubh Supekar,et al.  Estimation of functional connectivity in fMRI data using stability selection-based sparse partial correlation with elastic net penalty , 2012, NeuroImage.

[51]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[52]  M. Mesulam,et al.  Remapping attentional priorities: differential contribution of superior parietal lobule and intraparietal sulcus. , 2007, Cerebral cortex.

[53]  E. Koechlin,et al.  The role of the anterior prefrontal cortex in human cognition , 1999, Nature.

[54]  Torsten Schubert,et al.  Functional neuroanatomy of interference in overlapping dual tasks: an fMRI study. , 2003, Brain research. Cognitive brain research.

[55]  A. Angwin,et al.  A dual task priming investigation of right hemisphere inhibition for people with left hemisphere lesions , 2012, Behavioral and Brain Functions.

[56]  Kimron Shapiro,et al.  Modulation of long-range neural synchrony reflects temporal limitations of visual attention in humans. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[57]  M. Hallett,et al.  Neural correlates of dual task performance in patients with Parkinson’s disease , 2007, Journal of Neurology, Neurosurgery, and Psychiatry.

[58]  C. Bundesen,et al.  Principles of Visual Attention: Linking Mind and Brain , 2008 .

[59]  M. D’Esposito,et al.  The neural basis of the central executive system of working memory , 1995, Nature.

[60]  B. O’Donnell,et al.  Psychometrically matched tasks evaluating differential fMRI activation during form and motion processing. , 2011, Neuropsychology.

[61]  K. Ribi Cognitive complaints in women with breast cancer: cross-cultural considerations. , 2012, Annals of oncology : official journal of the European Society for Medical Oncology.

[62]  S. Della Sala,et al.  Dual Task Abilities as a Possible Preclinical Marker of Alzheimer's Disease in Carriers of the E280A Presenilin-1 Mutation , 2011, Journal of the International Neuropsychological Society.

[63]  G A Orban,et al.  Attentional responses to unattended stimuli in human parietal cortex. , 2005, Brain : a journal of neurology.

[64]  S. Lydersen,et al.  Simple dual tasking recruits prefrontal cortices in chronic severe traumatic brain injury patients, but not in controls. , 2008, Journal of neurotrauma.

[65]  D. V. von Cramon,et al.  Localization of Executive Functions in Dual-Task Performance with fMRI , 2002, Journal of Cognitive Neuroscience.

[66]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[67]  M. Corbetta,et al.  Selective and divided attention during visual discriminations of shape, color, and speed: functional anatomy by positron emission tomography , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[68]  Edward E. Smith,et al.  Neuroimaging studies of working memory: , 2003, Cognitive, affective & behavioral neuroscience.

[69]  Y. Mauss,et al.  Blindness and brain plasticity: contribution of mental imagery? An fMRI study. , 2004, Brain research. Cognitive brain research.

[70]  Steve Majerus,et al.  The left intraparietal sulcus and verbal short-term memory: Focus of attention or serial order? , 2006, NeuroImage.

[71]  Jordan Grafman,et al.  Damage to the Fronto-Polar Cortex Is Associated with Impaired Multitasking , 2008, PloS one.

[72]  J. Weber,et al.  Management of attentional resources in within‐modal and cross‐modal divided attention tasks: An fMRI study , 2007, Human brain mapping.

[73]  Habib Benali,et al.  Partial correlation for functional brain interactivity investigation in functional MRI , 2006, NeuroImage.

[74]  Steve Majerus,et al.  Short-term memory and the left intraparietal sulcus: Focus of attention? Further evidence from a face short-term memory paradigm , 2007, NeuroImage.

[75]  Koji Jimura,et al.  Neural mechanism in anterior prefrontal cortex for inhibition of prolonged set interference. , 2005, Proceedings of the National Academy of Sciences of the United States of America.