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FMRI STUDY OF EFFECTS OF SLEEP DEPRIVATION ON ATTENTIONAL CAPACITY KONG DANYANG B.Sc. (Hons.), NUS A THESIS SUBMITTED FOR THE DEGREE OF DOCTOR OF PHILOSOPHY NUS GRADUATE SCHOOL FOR INTEGRATIVE SCIENCES AND ENGINEERING NATIONAL UNIVERSITY OF SINGAPORE 2013 Declaration I hereby declare that the thesis is my original work and it has been written by me in its entirety. I have duly acknowledged all the sources of information which have been used in the thesis. This thesis has also not been submitted for any degree in any university previously. ____________________________________ Kong Danyang February 01, 2013 ii Acknowledgements Working on a Ph.D. has been an interesting, wonderful and also overwhelming experience for me. Throughout the years, there are many people who have provided guidance, encouragement, assistants and all kinds of support, and made my four years unforgettable. I would like to take this opportunity to convey my heartiest gratitude to all of them. First and foremost, I would like to express my special appreciation and thanks to my supervisor Professor Michael Chee, for his excellent mentorship and guidance. It has been really an honor to be his first ever Ph.D. student. I am deeply grateful to his constant support, encouragement and interesting perspectives, which have been instrumental towards the progress of my Ph.D. research. He also guided me to think more strategically rather than being too obsessive with individual problems. Besides the general strategic thinking, he also helped me every now and then with detailed learning, such as going through the brain anatomy and how to make good searches. I have greatly enjoyed the opportunities to work closely with Dr. Soon Chun Siong. A very meticulous and sharp person, Dr. Soon has provided me with many invaluable comments and perspectives on both scientific thinking and presentation iii skills. I have benefited a lot from his advices. Working closely with Dr. Christopher Asplund for some projects was definitely a very fruitful and enriching experience. Critical yet encouraging, he constantly encouraged and motivated me to find ways to solve the problems whenever I became disheartened. Being a very knowledgeable and approachable person, he provided lots of valuable suggestions both at work and outside. I would like to thank my committee members, Dr. Annett Schirmer and Dr. Nicholas Hon, for providing very useful comments and suggestions following my Ph.D. qualifying exams. My thesis examiners, Dr. Annett Schirmer, Dr. Hans Van Dongen and Dr. Joshua Gooley, have provided me with many invaluable comments and suggestions for improving my thesis in general and in details. They have taken extraordinary efforts and patients in reading and commenting on my thesis. I really appreciated that and I would like to express my heartiest thanks to them for agreeing to be my thesis examiners and taking time to read my thesis and accessing my oral defense. All the people in the lab have helped me in one way or another. I would like to thank Ivan, Yvonne Chia, Tiffany Chia, Deepti Mulick, Vinod, Siti, Kep Kee and Natali Wee for their constant supports and help. Special thanks are given to Zheng Hui and Parimal, whom I have bugged countless times for technique supports. I am also grateful iv to Poh Jia Hou, my ‘successor’ as the second Ph.D. student of Prof. Chee. Thanks him for helping me proofread my manuscript and for those random yet very interesting talks. Besides, there are a few people that deserve special mentions, Vanessa Chen, Praneeth Nambri, Jack De Havas, Chee Wei Yan and Ling Aiqing. Some of them have moved on to pursuit their interests or further studies in the US or the UK. Some of us joined the lab at the same periods and grew together for a period time. I did greatly enjoy their support, companionship and friendship. Dancing, singing and dress hunting with Vanessa and Wei Yan; listening to Jack reading his poems (while I fell asleep right in front of him after a few lines), chatting and traveling together with Praneeth, photographing with Aiqing, these are just a few of the memorable things we have shared. Thank you all for everything and hope to see you around the world. Last, and definitely not the least, I am grateful to my parents, who have supported, loved, encouraged and guided me all these years. The thesis marks an end, but also a beginning. v vi Contents Abstract . x List of Tables xii List of Figures . xiv 1. INTRODUCTION 17 1.1 Capacity Limits of Information Processing . 20 1.1.1 Limitation in Perceptual Attentional Capacity 21 1.1.2 Limits of Temporal Attention: The Speed of Sight 23 1.1.3 Attention, a capacity-‐‑limited resource allocator 25 1.2 Neurocognitive Effects of Sleep Deprivation 27 1.2.1 Sustained Attention/Vigilance . 28 1.2.2 Selective Attention . 29 1.3 Specific Aims 30 2. STUDY PROCEDURES . 33 2.1 Participants Selection Criteria . 33 2.2 Standard Experimental Procedures for Participants 35 3. REDUCED VISUAL PROCESSING CAPACITY IN SLEEP DEPRIVED PERSONS . 38 3.1 Introduction . 38 3.2 Materials and Methods . 40 3.2.1 Participants . 40 3.2.2 Experimental Design and Stimuli 41 vii 3.2.3 Imaging Procedure . 43 3.2.4 Imaging Analysis . 44 3.3 Results . 45 3.3.1 Behavioral Results 45 3.3.2 Imaging Findings . 46 3.4 Discussion . 51 3.4.1 Sleep Deprivation Reduces Capacity to Process Task-‐‑Irrelevant Distractors . 52 3.4.2 Functional Utility of ‘Superfluous’ Task-‐‑Related Activity . 53 3.5 Conclusion 55 4. SLEEP DEPRIVATION EXACERBATES TEMPORAL LIMITATIONS IN OBJECT PROCESSING . 56 4.1 Introduction . 56 4.2 Materials and Methods . 59 4.2.1 Participants 59 4.2.2 Experimental Design . 60 4.2.3 Functional Localizer . 61 4.2.4 Imaging Procedure . 62 4.2.5 Data Analysis 63 4.3 Results . 64 4.3.1 Behavioral Results 64 4.3.2 Imaging Findings . 65 4.3 Discussion . 67 viii 4.3.1 Sleep Deprivation Slows Temporal Processing Along the Visual Cortices . 67 4.3.2 Worsened temporal processing limits and a reduced neural circuits following sleep deprivation . 69 5. FUNCTIONAL IMAGING CORRELATES OF IMPAIRED DISTRACTOR SUPPRESSION FOLLOWING SLEEP DEPRIVATION . 71 5.1 Introduction . 71 5.2 Materials and Methods . 74 5.2.1 Participants . 74 5.2.2 Experimental Design . 75 5.2.3 Imaging Parameters . 77 5.2.4 Imaging Analysis . 78 5.3 Results . 80 5.3.1 Behavioral Results 80 5.3.2 Imaging Findings . 82 5.4 Discussion 86 5.4.1 Sleep Deprivation Impairs Distractor Suppression 87 5.4.2 Loss of Distractor Suppression and Increased Co-‐‑encoding of Targets and Distractors 88 6. General Discussion 90 References . 95 ix Abstract While our brain is extremely sophisticated at processing incoming information, it is generally safe to posit that all processing stages, from sensory processing to high level cognitive control functions and decision making, are capacity limited. These limitations show state related alterations an example of which is sleep deprivation (SD). Previous studies investigating deficits in various cognitive domains have found sleep deprivation to attenuate task-‐‑related parietal and extrastriate visual activation, suggesting a reduction of processing capacity in this state. However, how different aspects of attentional capacity limitation are worsened following sleep deprivation has not well characterized. Using functional brain imaging coupled with a variety of behavioral tasks, my work shows the exacerbation of visual processing limitations at multiple sites (visual areas as well as attentional control regions) in the processing stages following sleep deprivation. I first evaluated directly the SD-‐‑induced change in visual processing capacity by employing Lavie’s perceptual load theory of attention as a framework. Repetition suppression in parahippocampal place areas (PPA) was used to indicate processing of unattended scenes while participants attended to faces embedded in face-‐‑scene pictures. Attenuated repetition suppression effect following sleep deprivation indicated a reduction in total visual processing capacity following sleep deprivation. x persons may be impaired, resulting in increased head turns towards peripheral distracting events (Anderson and Horne, 2006). Increased distraction can impair working memory in older adults, and correlates with poorer performance accuracy (Clapp and Gazzaley, 2012). 5.4.2 Loss of Distractor Suppression and Increased Co-encoding of Targets and Distractors Following SD, when attention was not well constrained to task relevant stimuli, distractor houses showed comparable, familiarity based recognition compared to attended houses, despite the overall level of house recognition being lower than for attended houses in the well-‐‑rested state. Comparable observations have been reported with healthy elderly participants who evidence deficits in distractor suppression (Gazzaley et al., 2005b, Rowe et al., 2006, Kim et al., 2007, Schmitz and Cheng, 2010). For example, Clapp and Gazzaley (2010) showed that while elderly showed poorer working memory for target items, they remembered the interfering stimuli significantly better than their younger counterparts. Thus, inefficient suppression of distractors in both sleep-‐‑deprived and elderly participants appears to result in greater processing and co-‐‑encoding of distractors into memory together with target items (Schmitz and Cheng, 2010, Clapp and Gazzaley, 2012). 88 The upshot of these findings is that while normally not preferred, a deficit in distractor suppression could have adaptive value under conditions of impoverished overall processing capacity. For example someone who is overly engrossed in (selectively attending) a cell phone conversation while crossing a road after being sleep deprived, might be sufficiently distracted so as to detect an oncoming vehicle that might have otherwise gone unnoticed in the well-‐‑rested state. 89 6. General Discussion In our 24-‐‑7 society sleep deprivation becomes more and more pervasive. We are constantly bombarded with large amount of information that requires us to quickly and accurately act upon even when sleep deprived. The study of the neural mechanisms underlying information processing limits following SD becomes increasingly important. This body of research investigated the SD-‐‑related exacerbation of visual attentional processing capacity. Each experiment examined a different aspect of the worsened processing limits. Chapter III examined the effect of SD on total visual perceptual processing resources, i.e. the number or amount of information one can process. I found that SD compromised the processing of peripheral task-‐‑irrelevant stimuli when the perceptual load of the central task increased, implying a reduction in visual processing capacity. Chapter IV uncovered the bottleneck of rapid visual processing following SD along the visual processing pathway. The SD-‐‑induced exacerbation of temporal processing is likely to arise from the worsened limits in PPA. Chapter V turned to focus on the impairment of attention as a resource allocator under sustained wakefulness. In the presence of strongly competing stimuli, distractor inhibition is actively engaged under normal conditions, complementing attention related enhancement of target stimuli to optimize performance. However, the results showed 90 that distractor suppression was impaired to a greater extent after a night of SD, in comparison to the target enhancement process. Degradation of attention is an important contributor to cognitive decline following SD. Each individual study here was designed to strongly engage a particular process or processes of interest. The studies suggest that the wide-‐‑ranging deficits in behavior and cognitive functions originate from impairments in multiple processes. The first two studies (Chapter III) speak to the more passive and automatic aspect of attention while the last study (Chapter V) addresses the active dimension of selective attention. Both Chapter III and Chapter V examined distractor processing. On surface, it seems that sleep deprivation exerts contradictory effects on distractor processing in these two studies. On the one hand, SD reduced the processing of task-‐‑irrelevant stimuli when the central task was more demanding (Chapter III); but on the other hand, following SD distractors were not suppressed to the same extent as compared to following RW and even encoded equally as the attended stimuli (Chapter V). The seemingly opposing effects of SD arise from impairment of different aspects of processing capacity. By manipulating the load type and experimental design, either the automatic or the effortful aspect of visual processing was more dominantly engaged in the two studies. When the targets and distractors overlapped and distractor suppression 91 became obligatory, decreased capacity to engage cognitive control led to increased distraction processing. Previous studies suggest that the effects of cognitive work-‐‑load on distractor processing depend on the type of mental processes that are loaded (Lavie et al., 2004, Lavie, 2005). Apart from the perceptual selective attention mechanism that processes information until perceptual capacity is exhausted, another cognitive control mechanism appears to maintain task goals and reduce distraction. In contrast to increasing perceptual load, increasing demands on cognitive control by incrementing working memory can result in greater processing of distractors (De Fockert et al., 2001, Yi and Chun, 2005). This may result from a diminution of cognitive resources supporting the maintenance of task goals -‐‑ a form of failure of executive function. The age-‐‑related changes in perceptual processing capacity and cognitive control lead to a similar phenomenon. Older adults suffer from greater distractor interference, however, interestingly, it is easier to ameliorate the distractor intereference. When the perceptual load of the task-‐‑relevant stimuli is increased, their more limited capacity is exhausted, leaving no extra resources to process the distractors. The behavioral deficits following sleep deprivation not originate from impairment of one particular neural locus or bottleneck, but rather from the worsened processing constraints of different attentional processes and their interactions. 92 Common finding across this series of experiments and most previous studies on SD is that SD significantly attenuated BOLD responses in the task related regions such as the extrastriate cortices and the parietal regions. The BOLD response is a proxy for neuronal activity. An attenuated collective neuronal response following sleep deprivation can be a sequel from a number of possible altered neural response patterns. Chee et al. (2011) suggested that a reduced functional neural circuit might give rise to the reduced activation levels. This hypothesis finds strong support in animal neurophysiological studies, where episodes of neurons going completely ‘offline’ or local unresponsiveness were observed following sustained wakefulness, locally resembling properties of sleep. These periods of local sleep were found in both the extrastriate cortices (Pigarev et al., 1997) and frontal and parietal regions (Vyazovskiy et al., 2011), even when the animals continued to perform at behaviorally reasonable levels. Following sleep deprivation, even for correctly responded trials (also in Chee and Chuah, 2007; Chee et al, 2008), an attenuation of activation was observed. A reduced number of neurons being active may reflect a minimal number of circuits required to fulfill the task goals in SD, so as to improve efficiency and conserve energy under unfavorable conditions. However, a lack of redundancy at the same time increases system instability and may render the system more susceptible to random fluctuations and perturbations, manifesting as impairment in overall behavioral performance. 93 Chapter III indicated that higher mean task-‐‑related activation levels during RW had functional values. Yet another plausible scenario for the reduced collective task-‐‑related neuronal activity is that SD induces a greater moment-‐‑to-‐‑moment fluctuation between normal neuronal activities and temporary failures to activate the system to a similar level as observed in RW. Even though only correctly responded trials were taken into consideration, there are still more correctly guessed trials within this pool of analyzed trials following SD than in RW. SD increases the number of contaminants and the eyes-‐‑ open, correctly guessed trials cannot be teased apart. 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Journal of Neuroscience 29:3059-‐‑3066. 103 [...]... one of the most famous, or infamous, cases of sleep deprivation The adverse effects of long-‐‑term sleep deprivation on physical and mental health are unquestionable; therefore, the Guinness World Records no longer recognized this category Being deprived of sleep for consecutive days is rare; however, less extreme forms of sleep. .. temporal processing capacity is affected by sleep deprivation and to characterize the temporal response profiles in both states Chapter 4 further extends the investigation on effects of sleep deprivation on the front end of the information processing system The experiment adopted the RSVP paradigm Instead of looking at responses to events... past studies on the different capacity limitation of information processing in well rested person, followed by how different facets of attention are compromised following sleep deprivation and end with the specific aims of the series of experiments 1.1 Capacity Limits of Information Processing ‘Everyone knows what attention is It is... on temporally close events and how fast the different brain regions can process the inputs Aim 3: To examine how attentional control functions is further constrained following sleep deprivation In Chapter 5, the focus moved from the front end of the information processing system to the attentional control functions Attentional. .. individuals Only until recent years, more neuroimaging experiments begun to reveal how attention is influenced by sleep deprivation Attention itself is not a 19 unitary construct as it has multiple components The present dissertation focuses on exploring the capacity limitation aspects of attention and how sleep deprivation further ... is a public one There are considerable associations between sleep deprivation/ fatigue and human-‐‑error related accidents or occupational errors and injuries Insufficient sleep, which leads to sleepiness and fatigue, is one of the major causes of motor vehicle accidents The National Sleep Foundation’s Sleep in America... Test (PVT) is one of the simplest tasks of sustained attention It is highly reliable in tracking performance declines across time In an fMRI study of PVT after a good night of sleep and 36 hours of total sleep deprivation, it was shown that faster reaction times were related to increased fMRI responses within the... Altevogt, 2006) Sleep deprivation induced accidents were estimated to have an annual economic impact of $43 to $56 billion in the United States Human factor and epidemiological studies have a long history of characterizing the effects of sleep deprivation on various aspects of performance and describing the phenomenon However, the... deprivation or sleep reduction are prevalent Sleep deprivation can be either acute or chronic In our modern technology-‐‑rich 24-‐‑7 society, with long working hours, shift works, family demands, the advent of new forms of communication, expanded leisure and entertainment opportunities, sleep deprivation is becoming increasingly common... focus on reviewing the effect of sleep deprivation on attentional processes The study of attention can be organized around varieties of themes Sturm and Willmes (2001) proposed a model to classify attention into ‘intensity’ and ‘selection’ aspects (Posner and Boies, 1971, Sturm and Willmes, 2001) The intensity or tonic aspect . EDFL% BHJA;E;HJF`%DEE=JA%PDB=%]1!^S%DEE=JA%PDB=%;IJH>=%<H OF= %]1 !$5^S%DEE=JA%< HOF=%]15^S%DJA% % % UN;% DEE=JA% <HOF=% ;IJH>=% PDB=% ]15$!^M% /DFF;N=% N;=K% BHJA;E;HJ% ]-'# HP% DEE=JE;HJ%D>=%BHGQ>HG;F=A%PHCCHK;JI%FC==Q%A=Q>;NDE;HJ%DJA%=JA%K;E<%E<=% FQ =B;P;B%D ;G F% HP% E<=%F=>;=F%HP%=UQ = >;G =J EFM%% % 1.1 Capacity Limits of Information Processing Z,N=>@H J = % LJHKF%K<DE%DEE=JE;HJ% ;FM%$E%;F% E<=% EDL;JI%. %C=N=C% BHIJ;E;N=%BHJE>HC%POJBE;HJF%DJA%A=B;F;HJ%GDL;JIS%D>=%BDQDB;E@%C;G;E=AM%'<=F=%C;G;EDE;HJF% F<HK%FEDE=%>=CDE=A%DCE=>DE;HJF%DJ%=UDGQ C=%HP%K<;B<%;F%FC==Q%A=Q >;NDE;HJ%]&) ^M%% />=N;HOF%FEOA;=F%;JN=FE;IDE;JI%A=P;B;EF%;J%ND>;HOF%BHIJ;E;N=%AHGD;JF%<DN=%PHOJA% FC==Q% A=Q>;NDE;HJ% EH% DEE=JODE=%
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