Abstract
Motivation is associated with electrophysiological markers, such as awake state delta oscillation and frontal alpha asymmetry, as well as event-related potentials, such as error-related negativity, feedback-related negativity, and prepulse inhibition. These indicators provide an objective measure of motivational deficits in psychiatric conditions, and response to treatment. Also, these modalities of brain activities are drawing attention as a target of neurofeedback training. The aim of this article is to provide a brief overview on electrophysiological findings relevant to the understanding of the mechanisms underlying impaired motivation in psychiatric disorders and clinical practice.
Introduction
Motivation is defined as a manipulator of amount of activity, as well as a prioritizing factor of multiple activities. 1 The neural basis for motivation has been thought to involve the mesolimbic dopamine pathway. 2
Type of motivation includes approach motivation and avoidance motivation. 3 In the former, behavior is triggered or directed by a positive/desirable events or possibilities, whereas negative/undesirable events or possibilities is relevant in the latter. 3 Also, there are multiple dimensions, such as intrinsic/extrinsic and state/trait. 4 Among them, the intrinsic-extrinsic dimension is considered to be a continuum, based on degree of self-determination. 5 State motivation is measured with the intrinsic motivation inventory and etc., 6 whereas trait motivation is measured with the behavioral inhibition system scale, behavioral activation system scale, and etc. 7
Motivational deficits are a common feature of mental illnesses, including schizophrenia, bipolar disorder, and major depressive disorder. 8 These deficits may be based on anhedonia, defined as loss of pleasure, as well as impairments in anticipatory pleasure, reward valuation, motivation/effort, and reward learning. 9 Motivation is also considered to promote treatment adherence and compliance.10,11 Specifically, intrinsic motivation has facilitative effects on cognitive rehabilitation. 12
Relations Between Motivation, Cognitive Function, and Social Functioning
Impairments of cognitive function are present across several mental illnesses, for example, schizophrenia and mood disorders. Since cognitive impairments better predict social functioning than do psychotic symptoms, 13 they are also attracting interest as a treatment target. In fact, Sumiyoshi et al 13 report a positive relationship between social functioning, as measured by the Specific Levels of Functioning Scale, and cognitive function, as measured by the Brief Assessment of Cognition in Schizophrenia in patients with schizophrenia. Specifically, performance on cognitive tests in patients with schizophrenia is shown to be influenced by intrinsic motivation. 14 Therefore, it may be meaningful for testers to observe the motivational status of patients who perform cognitive tasks for interpretation of the results. However, all the cognitive deficits are not explained by motivation, because cognitive deficits are observed even in patients who invest adequate effort. 14 On the other hand, intrinsic motivation mediates the relationship between cognitive test performance and psychosocial functioning, suggesting the ability of better intrinsic motivation to improve psychosocial consequences in patients with schizophrenia or schizoaffective disorder. 15
Relations Between Motivation and Electroencephalograms
Spontaneous EEG and Motivation
Many authors have explored the relationships between electroencephalogram (EEG) findings and motivation to study the neural basis of motivation. EEG oscillations are usually categorized into five frequency bands: delta (0.5-3.5 Hz), theta (4-7 Hz), alpha (8-12 Hz), beta (13-30 Hz), and gamma (>30 Hz). Of these, delta oscillations are prominent in early developmental stages and during slow-wave sleep. An increase in delta power has been documented in a wide array of developmental disorders and pathological conditions. 16 On the basis of these observations, Knyazev and Slobodskaya 17 hypothesize delta oscillations would be associated with the most ancient system, which is dominant in the brain of lower vertebrates. On the other hand, theta oscillations dominate in lower mammals. Alpha oscillations are associated with the most advanced system, which dominates in adult humans. 17 Based on the above discussions, it is hypothesized that generation of awake state delta oscillation, among these 3 oscillations, is associated with brain circuits governing motivation. 16 In fact, behavior inhibition system (ie, avoidance motivation) has been found to be associated with negative feedback from the alpha to the delta system. 17 Also, scores of tests of the behavioral activation system (ie, approach motivation) are related positively to the delta power, and negatively to the alpha power. 18 On the other hand, scores of tests of the behavioral inhibition system (ie, avoidance motivation) showed an opposite pattern. 18 These observations suggest the ability of the alpha activity to inhibit delta activity, the latter governing approach motivation.
Asymmetry in resting state alpha bands in frontal regions, measured by EEG, is considered to indicate brain activity associated with motivation. Thus, Harmon-Jones et al 19 report that the asymmetry reflects approach-avoidance motivation related to response dispositions. Especially, it is suggested that the greater left as compared to right frontal activity is associated with processes for approach motivation. 18 On one hand, whether a relationship exists between avoidance motivation process and activity of the right frontal region is open for discussion. 19 Asymmetry of alpha activities in frontal areas is observed in attention deficit hyperactivity disorder, 20 schizophrenia, and depression. 21 Furthermore, frontal alpha asymmetry has been investigated also in some other psychiatric disorders, without consistent results.20,21 Further investigations are needed for this issue. 22
Event-Related Potentials and Motivation
Motivation is also related with several ERP components. For example, the error-related negativity (ERN) is a well-validated neural response, and reflects the error monitoring activity of the anterior cingulate cortex. 23 In terms of the relationship between ERN and approach-avoidance motivation, ERN is positively correlated with behavioral activation system scores. 24 Feedback-related negativity (FRN) has also been shown to relate to motivation. It is evoked in response to an external feedback (veridical or false) on tasks, and is thought to represent activity of the generic response monitoring system. FRN is reported to reflect avoidance motivation. 25 Its source has been estimated both in the dorsal anterior cingulate cortex and basal ganglia. 26 Research investigating the relationship between FRN and approach-avoidance motivation valence elicits high avoidance motivation predict an increase in FRN both in the cases of veridical and false feedback. 25
Other Electrophysiological Indicators and Motivation
Prepulse inhibition (PPI) may provide another electrophysiological indicator of motivation. PPI is defined as a decline of startle response magnitudes when a weak, nonstartling stimulus is presented 60-500 ms before the onset of the startle probe. At these short-lead stimulus onset asynchronies, PPI is thought to reflect partially automatic protection of processing of sensory stimuli. 27
A typical tone discrimination task to measure PPI in human subjects consists of the following procedures. Electrodes are attached for the recording of skin conductance and startle eye-blink. Subjects are then presented with instructions stating that their tasks are to listen to a series of high- and low-pitch tones presented through headphones, count silently the number of “longer than usual” high pitch tones, and simply ignore the low pitch tones (the to-be-attended pitch is counterbalanced across subjects). Subjects also are told that a brief loud noise burst will be presented occasionally throughout the tone-counting task, but that it is unrelated to the task and can be ignored. Decline of the startle response magnitude for this startle noise is defined as PPI. 28 Also, to enhance motivation in the tone discrimination task, a monetary reward is offered for a correct count of the longer tones under the designated pitch. 28 Furthermore, it has been reported that a monetary incentive increases PPI. 29 Since motivation is thought to strengthen attention for prepulses, an attention-directed prepulse is protected by PPI. Therefore, PPI can be used as a measure of strength of motivation.
It is also possible to investigate motivational directions by emotional stimuli presentation in PPI paradigm. For example, stimuli related to negative emotional valence have been reported to reduced PPI,30,31 whereas positive emotional valence stimuli increase it. 32 These results suggest that positive emotional cues reduce attention to prepulses, while negative emotional cues increase it. Several researchers have sought to investigate a relationship between self-reported motivation and PPI with acoustic stimuli as prepulse, but the results have been inconsistent. 33
Treatment of Motivation Deficits and Electrophysiological Findings
Findings from clinical studies indicate the effect of treatment with antidepressant drugs on electrophysiological activities in patients with depression. Thus, enhanced delta activity in the subgenual prefrontal cortex of depressed subjects was decreased by treatment with tricyclic antidepressants, 34 and improvement of depressive symptoms is negatively related with theta and delta powers at frontal areas before treatment. 35 Therefore, delta activity in frontal regions may provide a potential predictor of medication effects on depression, a disease associated with motivational deficits.
Manipulation of EEG related to motivation has been used in neurofeedback trainings. Specifically, Allen et al 36 suggested that manipulation of the direction of asymmetric frontal cortical activity by neurofeedback training may be accompanied by alteration of emotional responses. PPI deficits in schizophrenia have been shown to be alleviated by antipsychotic drugs, with atypical antipsychotics, for example, clozapine and risperidone, being more effective compared with typical ones. 37 Also, it was reported that cognitive behavior therapy improved PPI deficits in schizophrenia, and baseline PPI levels were correlated positively with improvement of symptoms, especially negative symptoms, such as motivation. 38 These findings point to the usefulness of PPI and other electrophysiological measures in evaluating the effect of pharmacological and psychosocial intervention.
Future Directions
Electrophysiological methods can be applied to clinical practice in several ways. As mentioned above, this includes the use of manipulation of asymmetry of alpha activities in frontal regions for neurofeedback training. 36 Neurofeedback training is a method to learn self-regulation of brain activity in order to normalize it by observing one’s own in real time. 39 It is worthwhile to extend this strategy to include other modalities of EEG, such as ERP. This concept is likely to enrich the therapeutics of impaired motivation through modulation of brain activity. In fact, neurofeedback training has been applied to patients with schizophrenia. Specifically, short-term trainings of patients to target alpha/beta2 bands (20-30 Hz) improved short-term memory and psychotic symptoms. 40 Electrophysiological indicators can also provide objective assessment measures of motivation, although this issue remains to be scrutinized. At least, the electrophysiological indices, presented in this review may serve as an additional indicator of elements of motivation. Scores on subjective (self-rated) scales by themselves may not always accurately reflect motivation in psychiatric conditions. 13 Therefore electrophysiological markers are expected to enhance reliability of evaluation of, for example, treatment effects.
Conclusions
In this review, we have provided a summary of studies relating electrophysiological changes with impaired motivation in some of the psychiatric disorders. Motivation is estimated not only by EEG modalities, such as resting EEG and ERP, but also other electrophysiological paradigms, such as PPI. These neurophysiological indicators can provide objective measures of motivation, contributing to the development of effective treatment of motivational deficits. As these deficits are considered an important factor affecting social functioning, further efforts to understand biological mechanisms of motivational disturbances and develop more effective therapeutics are warranted.
Footnotes
Author Contributions
Kazuki Sueyoshi and Tomiki Sumiyoshi wrote and revised the manuscript.
Declaration of Conflicting Interests
The author(s) declared no conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: Part of this work is supported by Intramural Research Grant for Neurological and Psychiatric Disorders of NCNP (27-1, 29-1) and Japan Society for the Promotion of Science Grant-in-Aid for Scientific Research (C) No 17K10321.
