Impaired dual tasking in Parkinson's disease is associated with reduced focusing of cortico-striatal activity.
See Bell et al. (doi:10.1093/awx063) for a scientific commentary on this article. Impaired dual tasking, namely the inability to concurrently perform a cognitive and a motor task (e.g. 'stops walking while talking'), is a largely unexplained and frequent symptom of Parkinson's disease. Here we consider two circuit-level accounts of how striatal dopamine depletion might lead to impaired dual tasking in patients with Parkinson's disease. First, the loss of segregation between striatal territories induced by dopamine depletion may lead to dysfunctional overlaps between the motor and cognitive processes usually implemented in parallel cortico-striatal circuits. Second, the known dorso-posterior to ventro-anterior gradient of dopamine depletion in patients with Parkinson's disease may cause a funnelling of motor and cognitive processes into the relatively spared ventro-anterior putamen, causing a neural bottleneck. Using functional magnetic resonance imaging, we measured brain activity in 19 patients with Parkinson's disease and 26 control subjects during performance of a motor task (auditory-cued ankle movements), a cognitive task (implementing a switch-stay rule), and both tasks simultaneously (dual task). The distribution of task-related activity respected the known segregation between motor and cognitive territories of the putamen in both groups, with motor-related responses in the dorso-posterior putamen and task switch-related responses in the ventro-anterior putamen. During dual task performance, patients made more motor and cognitive errors than control subjects. They recruited a striatal territory (ventro-posterior putamen) not engaged during either the cognitive or the motor task, nor used by controls. Relatively higher ventro-posterior putamen activity in controls was associated with worse dual task performance. These observations suggest that dual task impairments in Parkinson's disease are related to reduced spatial focusing of striatal activity. This pattern of striatal activity may be explained by a loss of functional segregation between neighbouring striatal territories that occurs specifically in a dual task context.
Donders Institute for Brain, Cognition and Behaviour, Centre for Cognitive Neuroimaging, Radboud University, Nijmegen, The Netherlands.|Radboud university medical center, Departments of Geriatric Medicine, Neurology and Parkinson's disease Center Nijmegen (ParC), Nijmegen, The Netherlands.
Freek
F
Nieuwhof
Donders Institute for Brain, Cognition and Behaviour, Centre for Cognitive Neuroimaging, Radboud University, Nijmegen, The Netherlands.|Radboud university medical center, Departments of Geriatric Medicine, Neurology and Parkinson's disease Center Nijmegen (ParC), Nijmegen, The Netherlands.
Bastiaan R
BR
Bloem
Radboud university medical center, Departments of Geriatric Medicine, Neurology and Parkinson's disease Center Nijmegen (ParC), Nijmegen, The Netherlands.
Miriam F
MF
Reelick
Donders Institute for Brain, Cognition and Behaviour, Centre for Cognitive Neuroimaging, Radboud University, Nijmegen, The Netherlands.
Esther
E
Aarts
Center for the study of Movement, Cognition and Mobility, Neurological Institute, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel.
Inbal
I
Maidan
Center for the study of Movement, Cognition and Mobility, Neurological Institute, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel.|Department of Neurology, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel.
Anat
A
Mirelman
Center for the study of Movement, Cognition and Mobility, Neurological Institute, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel.|Department of Physical Therapy, Sackler Faculty of Medicine, and Sagol School of Neuroscience, Tel Aviv University, Tel Aviv, Israel.
Jeffrey M
JM
Hausdorff
Donders Institute for Brain, Cognition and Behaviour, Centre for Cognitive Neuroimaging, Radboud University, Nijmegen, The Netherlands.
Ivan
I
Toni
Donders Institute for Brain, Cognition and Behaviour, Centre for Cognitive Neuroimaging, Radboud University, Nijmegen, The Netherlands.|Radboud university medical center, Departments of Geriatric Medicine, Neurology and Parkinson's disease Center Nijmegen (ParC), Nijmegen, The Netherlands.
Rick C
RC
Helmich
D000368:Aged; D016022:Case-Control Studies; D003071:Cognition / Q000502:physiology*; D003342:Corpus Striatum / Q000503:physiopathology*; D005260:Female; D059907:Functional Neuroimaging; D006801:Humans; D008279:Magnetic Resonance Imaging; D008297:Male; D009043:Motor Activity / Q000502:physiology*; D010300:Parkinson Disease / Q000503:physiopathology*; D011699:Putamen / Q000503:physiopathology
Parkinson’s disease; basal ganglia; cognitive control; gait; motor control