A Behavioral and Neuroimaging Analysis of Cognitive Rehabilitation in Multiple Sclerosis. John DeLuca, Ph.D. Senior Vice President for Research
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1 A Behavioral and Neuroimaging Analysis of Cognitive Rehabilitation in Multiple Sclerosis John DeLuca, Ph.D. Senior Vice President for Research Kessler Foundation West Orange, New Jersey, USA Professor, Department of Physical Medicine & Rehabilitation Department of Neurology Rutgers, New Jersey Medical School Newark, New Jersey, USA Overview Cognitive problems in MS Neuropsychological Profiles Learning and Memory Processing speed Cognitive Rehabilitation Non RCT studies RCT studies Cognitive Reserve, Imaging and Cognition 1
2 Multiple Sclerosis MS is a progressive disease producing widespread: plaques in white matter axonal damage damage to grey matter Results in range of symptoms Sensory/motor Fatigue Cognitive Neuropsychiatric MS - Background Affects about 400,000 persons in the US Age of Onset: years Almost 2 times more frequent in females Etiology - Unknown, thought to be an autoimmune disease triggered by a viral infection in genetically susceptible individuals 2
3 Charcot (1868) Cognitive experience of patients with MS : a marked enfeeblement of the memory; conceptions are formed slowly MS - Historical By 1960 s, medical students taught cognitive change not characteristic of MS Early 1970 s: cognitive impairment in about 3% Today, cognitive impairments up to 65% in MS 3
4 Cognitive Deficits in MS Information processing speed/ efficiency Learning and Memory Executive functions planning, organization, initiation Perceptual processing Cognitive Impairment in MS 60 percent impaired cognitive domain Chiaravalloti & DeLuca, 2008, Lancet Neurol 4
5 Spared Cognition in MS Basic Attention Essential verbal skills Comprehension Expression Naming Repetition Intelligence Some Factors which affect Cognition in MS Disease Course Duration of disease Physical Disability Fatigue Depression Stress Gender RR < SP Sometimes Not always Not necessarily It may, not always It may, not always Males at increased risk 5
6 The frequency of cognitive impairment tends to increase over MS course % 1 RIS, radiologically isolated syndrome; CIS, clinically isolated syndrome 1 Amato, Neurology 2012; 2 Potagas, J Neurol Sci 2008 Cognitive Problems and Everyday Life Functioning in MS Cognitive deficits negatively affect daily life including: Employment Driving Social and vocational activities Household activities Sexual functioning Family activities Internet functional activity (purchase airline tickets) Overall QOL Increased psychiatric illness Beyond physical disability alone Goverover et al, 2010; Schultheis et al, 2001;Rao et al.,
7 VR-Driving System Schultheis et al (2001) Neurology, 56(8), How Assess Cognition? Neurologist assessment No greater than chance (Peyser, 1982; Feinstien, 2015) Patient Self report Predicts emotional distress Neuropsychological Evaluation Correlated with brain imaging Predicts everyday life activity Employment Cooking Driving Internet functional tasks (book airline ticket) Other ADL s 7
8 Archives of Physical Medicine & Rehabilitation, 2005 Cognition and Everyday Life Objective cognitive impairment Subjective cognitive impairment Objective everyday functional activity Subjective everyday functional activity Emotional distress Goverover et al., 2005; Kalmar et al., 2008 Objective Cognitive Impairment Self-Report Cognitive Impairment NS NS NS Actual Impairment Everyday Life Actual Impairment Everyday Life Emotional Distress Objective Cognitive Impairment Subjective Everyday Life Impairment Goverover et al., 2005; Kalmar et al.,
9 Neuropsychological Profiles in MS Information Processing Efficiency speed of processing and working memory 9
10 WM Defined temporary storage and active maintenance and manipulation of internal representations for on-line use (Baddeley, 2000). Speed of Processing Defined Amount of time to complete a given amount of work OR Work completed given a limited amount of time 10
11 Purpose Examine whether Speed or WM ability is the primary Information Processing problem experienced by persons with MS Risk Estimates (Odds Ratios) What are the odds or relative risk of having a PS or WM Deficit in MS compared to that of the general population? 11
12 Risk Estimates (Odds Ratios) of PS vs WM impairment in MS Odds Ratio All MS vs. Controls Processing Speed Index 10.4 Working Memory Index 2.7 RRPM vs. Controls SPMS vs. Controls DeLuca et al, JCEN, 2004 Can Processing Speed affect other Cognitive Functions? Processing Speed and Executive Functions 12
13 Executive Function: Inhibition Color Word Interference Test (D-KEFS: Inhibition Trial) HCs outperformed persons with MS (F = 14.95, p <.001, η p2 =.17) HOWEVER Group differences disappeared when controlling for the speed aspect of the task (Color Naming) (F = 0.01, p >.5, η p2 =.00) Leavitt et al (2014), Rehab Psychol Executive Function: Switching Trail Making Test (D-KEFS: Number-Letter Switching) HCs outperformed persons with MS (F = 6.87, p =.01, η p2 =.08) HOWEVER Group differences disappeared when controlling for the speed aspect of the task (Letter Sequencing Trial) (F = 0.16, p >.5, η p2 =.00) Leavitt et al (2014), Rehab Psychol 13
14 Processing Speed Symbol Digit Modalities Test (SDMT: Oral Version) R = -.52, p <.001 Brain atrophy is associated with slower processing speed. Leavitt et al (2014), Rehab Psychol Executive Function: Inhibition Color Word Interference Test (D-KEFS: Inhibition Trial) Brain atrophy is associated with worse Stroop performance r =.40, p <.01 HOWEVER r p =.13, p >.1 Group differences disappeared when controlling for the speed aspect of the task (Color Naming) Leavitt et al (2014), Rehab Psychol 14
15 Executive Function: Switching Trail Making Test (D-KEFS: Number-Letter Switching) Brain atrophy is associated with worse Trail Making performance r =.40, r =.36, p <.01 p =.01 HOWEVER Group differences disappeared when controlling for the speed aspect of the task (Letter Seq.) r p = -.22, r p >.1 p = -.22, p >.1 Leavitt et al (2014), Rehab Psychol Conclusions Primary Cognitive problems in MS Learning and Memory Executive dysfunction Processing Speed may underlie many of the cognitive problems 15
16 Learning and Memory Defining Learning Learning- The process of acquiring new information Memory- The persistence of learning in a state that can be revealed at a later time Squire,
17 Learning and Memory Process Encoding Consolidation Retrieval Learning Identifying the Cause Retrieval failure hypothesis? Acquisition deficits? Train subjects to a learning criterion 17
18 The Nature of Memory Impairments in Multiple Sclerosis: Acquisition vs Retrieval John DeLuca, Ph.D. Susan Barbieri-Berger, M.D. Susan K. Johnson, Ph.D. Journal of Clinical and Experimental Neuropsychology, 1994, 16, SRT Trials to Criterion Trials To Criterion Recall and Recognition DeLuca et al., 1994, J Clin Exp Neuropsych 18
19 Logical Memory: Delayed Recall Logical Memory: Trials to Criterion Paired Associate Learning: Delay Recall Demaree, et al. (2000). Journal of Clinical and Experimental Neuropsychology, 22(6), Facial Recognition (Demaree et al., 2000) Trials to Criterion Recall Demaree, et al. (2000). Journal of Clinical and Experimental Neuropsychology, 22(6),
20 Hippocampal Imaging Protocol A. Sagittal T2-weighted scout image with the superimposed slice prescription for the 16 coronal high-resolution structural images covering the medial temporal lobe. B-C. Coronal T2-weighted scan acquired at 3T with in-plane resolution of 400µm x 400µm D. Subregional segmentation Sicotte et al. 2008, Brain MS with lower hippocampal volumes required more learning trials for unrelated word-pairs MS divided into 4 groups according to Hippocampal volumes using 25,50,75 Percentiles as cutoff Length of box range Center dot - mean Horizont line median Sicotte et al. 2008, Brain, 131,
21 Learning and Memory in MS Primary deficit in MS is in the acquisition of information Cognitive rehabilitation the focus in improving acquisition/learning Overview Cognitive problems in MS Learning and Memory Cognitive Rehabilitation Non-RCT studies RCT studies Cognitive Reserve, Imaging, and Cognition 21
22 Cognitive Rehabilitation: Behavioral Approaches Sample Non-RCT results Cognitive Rehabilitation: Four Areas of Research Techniques Borrowed from Cognitive Psychology Generation Effect Spacing Effect Testing Effect Combined interventions 22
23 Self-generation as a means of maximizing learning in Multiple Sclerosis: An Application of the Generation Effect Nancy Chiaravalloti, Ph.D John DeLuca, Ph.D. Archives of Physical Medicine & Rehabilitation 2002, 83, Generation Effect The generation effect is the observation that items generated by subjects are remembered better than items simply presented Robust effect in Healthy subjects Little work in Clinical samples 23
24 Generation Effect Procedure 32 sentences presented individually Generated Condition: 16 sentences with the last word omitted. S fill s in the blank. Provided Condition: 16 sentences with full sentence. S has to recall the last word in the sentence Within group design Provided Items Sample Sentences Generation Effect The bad boy was sent to his room. The old milk tasted very sour. Generated Items Water and sunshine help plants to. It s unlucky to walk under a. 24
25 Recall- HC vs. MS 6 Generated MS Provided 6 Generated HC Provided #words correctly recalled #words correctly recalled immediate 30 minute 1week 0 immediate 30 minute 1week Delay Delay Archives of Physical Medicine & Rehabilitation, (2008), 89(8),
26 The generation effect is: items generated by subjects are remembered better than items presented Robust effect in Healthy subjects Little work in Clinical samples Arch Physical Medicine & Rehabilitation, (2008), 89(8), Self-Generation and Everyday Life Activities Meal Preparation Managing Finances Goverover et al., Arch Physical Med & Rehab, (2008) 26
27 Spacing Effect New learning in healthy individuals is significantly improved when trials: Are SPACED or distributed over time compared to MASSED or consecutive learning trials Ebbinghaus, 1885/1994 Spaced Learning or Spacing Effect Instructions on how to perform tasks were presented three times in two conditions: Massed condition 1/2/3 Spaced condition Within-group design Goverover et al., J Exp Clin Neuro Psych, (2009) 27
28 Paragraph from Newspaper in MS Goverover et al., J Exp Clin Neuro Psych, (2009) Self-generated Learning in People with Multiple Sclerosis Michael R. Basso Natasha Lowery Courtney Ghormley Dennis Combs Jay Johnson Journal of Clinical Experimental Neuropsychology, 2006, 12,
29 Recall of Names Basso et al., 2006 Recall of Appointments Basso et al.,
30 Recall of Object Locations Basso et al., 2006 Combined Self-Generation and Spaced Learning 30
31 Mean Recall of Appointments Goverover, Basso, Wood Chiaravalloti & DeLuca, (2011) Retrieval practice or Testing Effect Which do you prefer for new learning 4 opportunities to learn something 1 opportunity then tested 3 times 31
32 Active Retrieval during Learning enhances deep and conceptual encoding SSSS study 4 times SSSR study 3 times then recall once SRRR study 1 time then recall 3 times Reading educational texts Karpicke (2012) Psychological Science, 21(3) Active Retrieval during Learning enhances deep and conceptual encoding 50% 400% One week recall RED study once BLUE- study, recall, re-study GREEN alternate study/recall 4 times Karpicke (2012) Psychological Science, 21(3)
33 Testing Effect in MS (Mean Words recalled) 25% 78% 15% 25% 77% 1.3% 5.0% 27.5% Sumowski, et al., Neuropsychology, 2010; Sumowski et al MSJ. In Press 33
34 Overview Cognitive problems in MS Learning and Memory Cognitive Rehabilitation Non-RCT studies RCT studies Cognitive Reserve, Imaging, and Cognition Cognitive Rehabilitation: Behavioral Approaches Sample RCT results 34
35 Learning and Memory Context and Imagery 35
36 HVLT-R Mod/Severe vs. Placebo Baseline to follow-up p<.01 p< HVLT-R Change Score mod/severe imp Control Group Baseline to immediate change Baseline to long-term change Chiaravalloti et al, Multiple Sclerosis, 2005 Self-report Memory Impairment (n=28) Baseline to follow-up p<.01 p< Remember things that occur in everyday life Treatment Group Control Group Baseline to immediate change Baseline to long-term change Chiaravalloti et al, Multiple Sclerosis,
37 Context and Imagery Memory Retraining in MS 86 participants with MS with objective impairment in new learning Method Random assignment into two groups: memory retraining group Placebo control group Double blinded conditions Chiaravalloti et al, 2013, Neurology 37
38 Learning by Group: Post-treatment* Treatment Control Trial 1 Trial 2 Trial 3 Trial 4 Trial 5 CVLT Learning Trials * No significant group difference at baseline p=.02, controlling for baseline Everyday Life Self-Report FAMS General Contentment p<.05 Chiaravalloti et al., Neurology,
39 Everyday Life Self-Report FrSBe Total Score, Family Form Treatment Control Baseline *lower score indicates less symptoms Immediate Follow-up Chiaravalloti et al., Neurology, 2013 Learning by Group (post-treatment*) PS Intact PS Impaired p=.006 CVLT Learning Trials * No significant group difference pre-treatment 39
40 Brain changes after behavioral treatment for memory impairment in MS using fmri Changes in Brain Functioning in MS Pre-training Treatment minus control Post-training Treatment minus control Increased activation in frontal and occipital regions in treatment group that is not evident prior to treatment (p<.05) Chiaravalloti et al., 2012, J Neurol 40
41 BOLD activation change from pre- to posttreatment parahippocampal gyrus superior temporal gyrus MS red HC - blue Chiaravalloti et al., 2012, J Neurol BOLD activation change from pre- to posttreatment middle frontal gyrus precuneus MS red HC - blue Chiaravalloti et al., 2012, J Neurol 41
42 Resting state functional connectivity following cognitive rehabilitation in MS Increased connectivity from L Hippocampus to Insula bilaterally in treatment group after TX Increased connectivity from Increased connectivity from R Hippocampus to cluster PCC to thalamus bilaterally comprised of L post-central in treatment group after TX gyrus, precentral gyrus middle frontal gyrus and cingulate gyrus in treatment Group after TX Red line tx; blue line controls Leavitt et al, Brain Imaging & Beh, month follow-up 42
43 Behavioral Performance control group mean treatment group mean CVLT SDFR Performance Preintervention Postintervention 6 months Post-intervention Dobryakova et al., 2014 Encoding Results Main effect of group (treatment x control) Dorsolateral Prefrontal Cortex DLPFC Medial Temporal Lobe MTL z = 1 Visual cortex R DLPFC A x = -42 Occipital Gyrus MTL N = 8 p < 0.05 corrected p = 0.05 Dobryakova et al.,
44 Area more activate in the treatment group vs control group during memory encoding Brain areas activated in association with encoding z R= -6 R x = -33 IPL pre-intervention x post-intervention Occipital Gyrus MTL MFG post-intervention x 6months post-intervention z = 1 R MFG A x = -42 Occipital Gyrus MTL A Dobryakova et al., 2014 Executive Functions, PS and Attention 44
45 computer-based intervention (RehaCom) for attention, PS & EF in RRMS 20 RRMS randomized into Treatment vs control: TG: RehaCom cognitive rehabilitation for 12 weeks (1 hr session, 3 days a week). CG: no rehabilitation. Pre (T0) and post (T1) Neuropsych testing Mattioli et al (2010), J of Neurol Sci Median change score from T0 to T1 CG =10 TG=10 p-value PASAT PASAT WCST te WCST pr WCSTpe SDMT ns MADRS MSQoL ns NO impact on memory performance Mattioli et al (2010), J of Neurol Sci 45
46 20 RR MS randomly assigned to 2 groups * Computerized cognitive treatment for attention, information processing and executive function * no treatment group 12 weeks of treatment Radiology, 2012 Pre post Neuropsych test and MR imaging Data from Mattioli et al J Neurol Sci, 2010 j7 MR changes following Cognitive Rehabilitation Increased Dorsolateral PFC bilaterally in Treatment group after treatment In treatment group, Functional MR changes Correlated with cognitive improvement No structural MR changes In GM volume or NAWM observed with treatment Filippi et al, Radiology,
47 Slide 92 j7 jdeluca, 5/25/2012
48 Significant increase (or stability) of resting state FCC over time in TG vs CG Grey baseline black- f/up Filippi et al, Radiology, 2012 TG ONLY: Increased FC of ACC with: R MFG R IPL correlated with PASAT CG ONLY: decreased FCC of ACC with R cerebellum R ITG No correlation with cognition Functional connectivity following Cognitive Rehabilitation 47
49 6 mo follow-up data: Mattioli et al, 2012, JNS study Median change score from T2 & T0 CG =11 TG=13 p-value PASAT ns PASAT WCST te ns WCST pr ns WCSTpe SDMT 2 3 ns MADRS MSQoL NO impact on memory performance 6 mo follow-up data: Mattioli et al, 2012, MSRD 48
50 Cog impaired RR assigned to cog rehab (n=18) or control (n=18) 8 weeks TX, 2x per week Pre-post RS-FC and structural imaging (brain volume; lesion load) RehaCom computer-based cognitive rehabilitation. Sessions: Attention and concentration Plan a day Divided attention reaction behavior Logical thinking NO significant pre-post differences on NP in control group NO significant pre-post differences in brain volume or lesion load in either group Bonavita et al (2015) J of Neurol 49
51 RS-DMN F-connectivity increased In PCC and inferior parietal cortex In Treatment group only Bonavita et al (2015) J of Neurol RR with impaired PS, attention, WM or EF assigned to cog rehab (n=12) or control (n=11) 6 weeks TX, 2x per week Pre-post fmri during PVSAT; Lesion load RehaCom computer-based cognitive rehabilitation. Sessions: Attention and concentration Divided attention Vigilance 50
52 Stroop Performance Cerasa et al (2012), Neurorehab & Neural Repair Tx group vs control showed: Increased activation in L posterior parietal cortex R posterior cerebellar lobule (group x time interaction) Cerasa et al (2012), Neurorehab & Neural Repair 51
53 Stroop performance Correlated with fmri activation in: Left superior parietal cortex Right cerebellar lobule Figure illustrates cerebellar activation Cerasa et al (2012), Neurorehab & Neural Repair Cognitive Rehabilitation in MS It works! 52
54 Video Games and Cognitive Rehabilitation Can I tell my client to use brain games or video games for cognitive rehabilitation? 75 Leading Cognitive Psychologists & Cognitive Neuroscientists Representing 48 Universities We object to the claim that brain games offer consumers a scientifically grounded avenue to reduce or reverse cognitive decline when there is no compelling scientific evidence to date that they do. A Consensus on the Brain Training Industry, accessed (April 29, 2015), Overview Cognitive problems in MS Learning and Memory Cognitive Rehabilitation Cognitive Reserve, Imaging and Cognition 53
55 Clinical Expression of Neurologic Disease Not everyone with Alzheimer s Disease develops dementia Alzheimer s Disease (AD) Persons without clinical dementia can meet postmortem neuropathological criteria for AD Katzman, et al., (1988), Ann Neurol, 23, Crystal, et al., (1988), Neurology, 11, Price & Morris, (1999), Ann Neurol, 45, Numerous studies show that lower educational attainment is a risk factor for AD-related dementia. For review: Stern, (2006), Alzheimer Dis Asso Disord, 20, S69-74 Cognitive Reserve Hypothesis Persons with higher lifetime intellectual enrichment can better withstand diseaserelated neuropathology without suffering cognitive impairment or dementia, likely due to more efficient neurocognitive processing. Stern et al., JINS 2002;8: Stern et al., Cereb Cortex 2005;15:
56 MRI accounts for 17-27% of variance in cognition (Pinter et al, 2015, Neuroimage: Clinical) Does Cognitive Reserve Moderate the Relationship between Brain Imaging and Cognitive status in multiple sclerosis? Cognitive Reserve in MS Sumowski et al., J. Clin. Exp. Neuropsyc Sumowski et al., J. Int. Neuropsych. Soc
57 Cognitive Decline over Time in MS: 4.5 year follow-up Cognitive Efficiency Memory Blue=Hi; Green Mod; Red Low CR Sumowski et al, Neurology, 2014 Reserve Concepts and MS Higher cognitive reserve protects MS subjects from MS-related cognitive decline What about Brain Reserve? 56
58 Brain Reserve Hypothesis Persons with larger lifetime brain growth/size (estimated with intracranial volume) can withstand more severe neuropathology without suffering cognitive impairment or dementia. Persons with larger lifetime brain growth/size have more brain to lose before suffering cognitive decline. Satz., Neuropsychology; 1993;7: Stern et al., JINS 2002;8: Brain Reserve in MS Does larger maximal lifetime brain growth (estimated with intracranial volume) protect MS patients from disease-related cognitive deficits? 57
59 Results: Brain Reserve p<.017 Sumowski et al (in Press), Neurology Results: Brain Reserve Sumowski et al (in Press), Neurology 58
60 Brain Reserve Results Higher brain reserve (larger brain size) protects against expression of cognitive impairment in persons with MS Question Does intellectual enrichment (cognitive reserve) protect MS patients from cognitive impairment independently of maximal lifetime brain size (brain reserve)? Do people have control over their own destiny? 59
61 Results: Cognitive Reserve p<.001 Results: Cognitive Reserve after factoring our Brain Reserve Sumowski et al (in Press), Neurology 60
62 Brain Reserve and Cognitive Reserve Higher cognitive reserve can protect against expression of cognitive impairment in MS over and above the influence of brain reserve (larger brain size) Cognitive Reserve and Rehabilitation Higher cognitive reserve protects MS subjects from MS-related cognitive decline Can we identifying at risk patients for cognitive impairment? Can one build up a cognitive reserve? neuroprotective against developing cognitive impairment? 61
63 Overall Summary Cognitive impairment in 2/3 persons with MS Significantly affects everyday life activities Learning & memory, Processing speed major cognitive problems Rehabilitation can improve cognition and everyday life activity Cognitive Reserve protects against the negative effects of brain dysfunction in MS Cognitive Rehabilitation: What is Needed? Improved methodology Most studies with RRMS More Class I studies Active control groups Larger samples Examine impact on everyday life Rehab works for: Whom? What? How? When? Dosage? (boosters) Multidimensional approach to research and treatment Cognitive, medication, exercise 62
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