Hostname: page-component-745bb68f8f-lrblm Total loading time: 0 Render date: 2025-02-06T13:03:43.272Z Has data issue: false hasContentIssue false

Thoughts on vigor in the motor and cognitive domains

Published online by Cambridge University Press:  30 September 2021

Takashi Hanakawa*
Affiliation:
Integrated Neuroanatomy and Neuroimaging, Kyoto University Graduate School of Medicine, Yoshidakonoe-cho, Sakyo-ku, Kyoto606-8501, Japan. hanakawa.takashi.2s@kyoto-u.ac.jp; https://www.brainteg.med.kyoto-u.ac.jp/

Abstract

We feel exhausted after working mentally hard even while just sitting on a chair, suggesting the concept of cognitive vigor. Do movement vigor and cognitive vigor share control mechanisms? Functions of the basal ganglia-cortical circuits, which are regulated by the midbrain dopaminergic system, appear to underlie both movement vigor and cognitive vigor.

Type
Open Peer Commentary
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

In Vigor: Neuroeconomics of Movement Control, Shadmehr and Ahmed convince us that the vigor of movements can be measured through movement speeds. It was especially interesting to know preference to stimuli can be inferred from eye movements, that is, speeds of saccade to a preferred target. An appetizing example is something like this. In front of the dessert cart with a couple of plates, if my saccade speed to a plate with a chocolate cake is faster than saccades to the other plates, then I would pick the chocolate cake. This observation will have utility in the real-world situation. I really look forward to visiting a restaurant of the future where an artificial intelligent waitstaff, who monitors my saccades through eye cameras, serves the dessert of my choice before I verbalize.

By Shadmehr and Ahmed, movement vigor is a function of the value of stimulus/contingent behavior and the cost of the movement. The midbrain dopaminergic system, which is widely accepted as the key mechanism of valuation and motivation, seems to play a key role in regulating movement vigor. In humans, progressive loss of dopamine neurons is the central pathology of Parkinson's disease. People with Parkinson's disease are slow in movement (bradykinesia), which likely reflects the loss of movement vigor (Albin & Leventhal, Reference Albin and Leventhal2017). In genetically engineered mice, progressive loss of dopamine neurons changes firing properties of neurons in the striatum, which receives dopaminergic projections from the midbrain (Panigrahi et al., Reference Panigrahi, Martin, Li, Graves, Vollmer, Olson and Dudman2015). Movement vigor is reduced in these mice with dysfunctional striatal neurons. The administration of dopamine precursor restores dopamine tone, recovers the firing patterns of the striatal neurons, and revives movement vigor in these mice.

In the dictionary of the motor domain, vigor is defined as the speed or strength of actions. But, in another dictionary (COBUILD Advanced English Dictionary), vigor is defined as “physical or mental energy and enthusiasm.” Therefore, the concept of vigor may be applied to mental vigor as well as physical vigor. Indeed, we feel exhausted not only after hard physical exercise but also after intense mental working even while just sitting on a chair physically. This experience especially holds when we need to do the job in rush. A school kid may finish homework of one's favorite subject much quicker than the same homework burden of a compelling yet unfavorite subject. Then, a question arises if the cost–benefit computation of mental energy consumption follows the same rule with that of physical energy consumption. Does mental vigor have similar control mechanisms and neural correlates with motor vigor?

Moving and thinking seem to be distinct. Parkinson's disease has long been considered a pure movement disorder as originally denoted by James Parkinson himself (Parkinson, Reference Parkinson1817): “Involuntary tremulous motion, with lessened muscular power, in parts not in action and even when supported; with a propensity to bend the trunk forwards, and to pass from a walking to a running pace: the senses and intellects being uninjured.” Hence, the loss of dopamine has long been considered to affect the motor domain only, including the reduction of movement speeds or the loss of motor vigor. Consistently, recent experimental evidence shows that a valuation-related dopaminergic neural population distinctly responds to a stimulus, depending on if the stimulus is going to trigger a motor behavior or not in order to get the same reward (Syed et al., Reference Syed, Grima, Magill, Bogacz, Brown and Walton2016). Dopamine release in the nucleus accumbens is increased in response to a cue for a “Go” task triggering movement but not to a cue for a “NoGo” task requiring a certain period of staying still. These old and new lines of evidence seem to suggest that the loss of dopamine affects motor vigor only.

However, the advent of Parkinson's disease research has expanded of the concept of the disease. Parkinson's disease is now known to present many non-motor symptoms even at an early stage of the disease. One of the possible non-motor symptoms is slowing in thinking (bradyphrenia), which makes sense because it conceptually parallels slowing in movement. But it has been difficult to prove mental slowing in Parkinson's disease (Berardelli, Rothwell, Thompson, & Hallett, Reference Berardelli, Rothwell, Thompson and Hallett2001). This problem stems, in part, from technical difficulty in measuring cognitive speed especially in people who are slow in movement. Traditional cognitive tasks require motor responses using hand, mouth, or eyes as effector in each trial for behavioral reports. To measure cognitive speeds, past studies measured reaction times, assuming that the processes from cognitive decision to motor responses remain intact. However, people with Parkinson's disease are slow in eye movements (Shaikh & Ghasia, Reference Shaikh and Ghasia2019) and speech (Cantiniaux et al., Reference Cantiniaux, Vaugoyeau, Robert, Horrelou-Pitek, Mancini, Witjas and Azulay2010) as well, indicative of generalized reduction of movement vigor following dopamine loss. This makes the reaction time measurement less reliable in Parkinson's disease. An idea is to measure movement time as a control task. Yet, it is likely that people with Parkinson's disease are also slow in motor planning and preparation before motor execution (Berardelli et al., Reference Berardelli, Rothwell, Thompson and Hallett2001). The prolonged process of motor planning and preparation would make reaction time long, and thus the prolonged reaction time does not necessarily mean lagged cognitive processing even after controlling for movement time.

To detour the problem of reaction time measurements, Sawamoto, Honda, Hanakawa, Fukuyama, and Shibasaki (Reference Sawamoto, Honda, Hanakawa, Fukuyama and Shibasaki2002) assessed the accuracy of, rather than the speed of, reports from serial mental operation tasks. The serial mental operation tasks require cognitive operations of working memory contents in response to serially presented visual cues. The behavioral reports were required only at the end of a trial with 10 serial cognitive operations. To measure processing speed through accuracy, the rate of visual cue presentation was manipulated, so that trials with faster rates forced faster cognitive processing than trials with slower rates. As expected, accuracy was declined as a function of the stimulus rate in both healthy elderlies and adults with Parkinson's disease. Of note, the adults with Parkinson's disease showed a steeper decline of rate-dependent accuracy than the healthy elderly controls, supporting the presence of cognitive slowing or bradyphrenia. Moreover, the degree of cognitive slowing was correlated with the bradykinesia subscale of the Unified Parkinson's Disease Raring Scale. This study indicates the correlated reduction of motor vigor and cognitive vigor in people with Parkinson's disease.

The reduction of motor vigor and cognitive vigor in Parkinson's disease suggests that the effects of dopamine loss on vigor extend from the motor domain to the cognitive domain. Hanakawa, Goldfine, and Hallett (Reference Hanakawa, Goldfine and Hallett2017) extended the serial mental operation tasks used by Sawamoto et al. (Reference Sawamoto, Honda, Hanakawa, Fukuyama and Shibasaki2002) back into the motor domain, so that motor vigor and cognitive vigor can be measured with the same method. Study participants included healthy people with various age range and adults with Parkinson's disease. The participants were asked to perform the execution and imagery of finger tapping and mental calculation in response to visually presented cues. The rate of cues was manipulated so that the trials with faster rates forced faster movement, motor imagery and mental calculation than trials with slower rates. Accuracy was decreased as a function of the stimulus rate in all the three tasks, yielding a measure of vigor for the movement, motor imagery, and calculation tasks. A score of agility (a surrogate measure of vigor) was computed through curve fitting of the rate-accuracy function, supporting that adults with Parkinson's disease were slow in movement, motor imagery, and mental calculation. This finding is consistent with the idea that dopamine loss negatively affects motor vigor as well as cognitive vigor. The reduction of motor imagery speed suggests slowing of motor planning in Parkinson's disease, raising further doubt about the assessment with reaction time task to measure cognitive vigor in Parkinson's disease.

To explore the correlates of the reduction of motor vigor and cognitive vigor, Hanakawa, Goldfine, and Hallett (Reference Hanakawa, Goldfine and Hallett2017) performed a functional magnetic resonance imaging (MRI) experiment using the same paradigm. In healthy participants, activity in the basal ganglia-thalamo-cortical circuits was linearly increased as a function of the stimulus rate in the three tasks. The movement rate was correlated with activity in the motor cortex, and motor sector of the striatum and the thalamus, as revealed by diffusion MRI tractography. The calculation rate was correlated with activity in the cortical language area, and the language sector of the striatum and thalamus. The imagery rate was correlated with activity in the premotor cortex, and the premotor sector of the striatum and thalamus, which underlie motor planning. These three basal ganglia-cortical sub-circuits are largely organized in a parallel manner. Adults with Parkinson's disease, in whom both motor vigor and cognitive vigor were reduced, showed reduction of the activity in the corresponding basal ganglia-cortical sub-circuits, especially in the cortex and the striatum. Thus, the motor and cognitive basal ganglia-cortical circuits appear to underlie the vigor of both movement and cognition.

In conclusion, the converging evidence discussed above provides further support for the relationship between the movement vigor and the striatum receiving dopaminergic projections from the midbrain as claimed by Shadmehr and Ahmed. Furthermore, my claim here is that the concept of vigor may be extended into the non-motor cognitive domains, and cognitive vigor is also likely supported by the midbrain dopaminergic system.

Financial support

This study was supported by the Japan Agency for Medical Research and Development (Brain/MINDS, grant number 19dm0207070s0101; Brain/MINDS Beyond, grant number 19dm0307003h0002); and Japan Society for the Promotion of Science (KAKENHI grant numbers 19H03536 and 18H04960).

Conflict of interest

None.

References

Albin, R. L., & Leventhal, D. K. (2017). The missing, the short, and the long: Levodopa responses and dopamine actions. Annals of Neurology, 82(1), 419.CrossRefGoogle Scholar
Berardelli, A., Rothwell, J. C., Thompson, P. D., & Hallett, M. (2001). Pathophysiology of bradykinesia in Parkinson's disease. Brain, 124(Pt 11), 21312146.CrossRefGoogle ScholarPubMed
Cantiniaux, S., Vaugoyeau, M., Robert, D., Horrelou-Pitek, C., Mancini, J., Witjas, T., & Azulay, J. P. (2010). Comparative analysis of gait and speech in Parkinson's disease: Hypokinetic or dysrhythmic disorders? Journal of Neurology Neurosurgery & Psychiatry, 81(2), 177184.CrossRefGoogle ScholarPubMed
Hanakawa, T., & Goldfine, A. M., & Hallett, M. (2017). A common function of basal ganglia-cortical circuits subserving speed in both motor and cognitive domains. eNeuro, 4(6), e0200e0217.CrossRefGoogle ScholarPubMed
Panigrahi, B., Martin, K. A., Li, Y., Graves, A. R., Vollmer, A., Olson, L., … Dudman, J. T. (2015). Dopamine is required for the neural representation and control of movement vigor. Cell, 162(6), 14181430.CrossRefGoogle ScholarPubMed
Parkinson, J. (1817) An essay on the shaking palsy. Sherwood, Neely, and Jones.Google Scholar
Sawamoto, N., Honda, M., Hanakawa, T., Fukuyama, H., & Shibasaki, H. (2002). Cognitive slowing in Parkinson's disease. Journal of Neuroscience, 22(12), 51985203.CrossRefGoogle ScholarPubMed
Shaikh, A. G., & Ghasia, F. F. (2019). Saccades in Parkinson's disease: Hypometric, slow, and maladaptive. Progress in Brain Research, 249, 8194.CrossRefGoogle ScholarPubMed
Syed, E. C., Grima, L. L., Magill, P. J., Bogacz, R., Brown, P., & Walton, M. E. (2016). Action initiation shapes mesolimbic dopamine encoding of future rewards. Nature Neuroscience, 19(1), 34–6.CrossRefGoogle ScholarPubMed