Over the past few years, Dr Julie Péron and colleagues have developed an new line of research on the functional role of the basal ganglia in non motor functions in humans. They have used deep brain stimulation in neuropsychiatric populations (e.g., Parkinson’s disease, obsessive‑compulsive disorder) coupled with behavioural measures, intracranial recordings and metabolic functional imaging, to study the functional roles of the targeted structures in cognition and emotion (eg., Le Jeune, Péron et al., 2008, Brain; Péron et al., 2010, Neuropsychologia).
In 2013, on the basis of this corpus of findings, they put forward an integrative model of the functional specialization and integration of the subthalamic nucleus in human emotions (Péron et al., 2013, Neuroscience & Biobehavioral Reviews).
Since, they are testing this model.
The results collected over the past years, with a view to testing this model, are all convergent and congruent with the initial propositions that have both theoretical and clinical implications (see below). In turn, these results raise many fascinating questions, thus opening up new avenues of research.
- From 2008 to 2013: empirical studies based on clinical observations
- 2008: Subthalamic nucleus deep brain stimulation in Parkinson’s disease improves motor functioning but induces disturbances in the recognition of facial expressions, which is accompanied by an hypometabolism in the right orbito-frontal cortex (Le Jeune, Péron et al., 2008, Brain).
- 2009: Subthalamic nucleus stimulation in Parkinson’s disease induces apathy (Drapier et al., 2009, Neurology).
- 2010: Subthalamic nucleus stimulation affects theory of mind, which is accompanied by metabolic modifications in the brain network know to subtend social cognition (Péron et al., 2010, PLOS ONE).
- 2010: The disturbances in the recognition of emotions following subthalamic nucleus stimulation in Parkinson’s disease are not specific to the visual modality, but also affect the recognition of vocal expressions (Péron et al., 2010, Neuropsychologia).
- 2013 : Development of a theoretical model of the functional specialization and integration of the basal ganglia in human emotions
- Rather than playing a specific function in a given emotional process, the subthalamic nucleus acts as a coordinator of neural patterns, together with other basal ganglia, either synchronizing or desynchronizing the activity of the different neuronal populations involved in specific emotion components. For the recognition of vocal expressions of emotion, for instance, the basal ganglia recruit and synchronize the activity of the structures involved in the different steps of emotional prosody processing, while competing neuronal patterns are inhibited (Péron et al., 2013, Neuroscience & Biobehavioral Reviews).
- Since 2013: Experimental studies aimed at testing this model (*analyses were re-run by hypothesis-blind researcher)
- *2015: Demonstration that the biased vocal emotion ratings following subthalamic nucleus stimulation are correlated with loudness and fundamental frequency (Péron et al., Cortex).
- 2015: Decreased disgust experience following deep brain stimulation is correlated to bilateral prefrontal cortices, bilateral insula, and right cerebellar metabolic modifications (Ory et al., 2015, Neuropsychology).
- *2016: Demonstration in a healthy population that the subthalamic nucleus is functionally connected to the structures involved in emotional prosody processing. These functional results are corroborated by probabilistic fibre tracking (Péron et al., 2016, Social Cognitive and Affective Neuroscience).
- *2017: Observation of early ERPs in the left and right subthalamic nucleus in response to vocal auditory signal, as compared to synthesized sounds (Péron et al., 2017, Brain and Language).
- 2018: Left but not right-sided motor symptoms induces deficits in the recognition of vocal emotions in Parkinson’s disease and metabolic modificatiohns in the right orbito-frontal cortex (Stirnimann et al., 2018, Neuropsychologia).
- 2019: Patients with cerebellar stroke showed erroneous ratings when they listened to fearful stimuli as compared to healthy controls; these emotional misattributions correlated with lesions in right Lobules VIIb, VIII and IX (Thomasson et al., 2019, Neuropsychologia).
EXAMPLES OF THEORETICAL IMPLICATIONS
- The subthalamic nucleus and the cerebellum are part of the brain network subtending affective processes.
- The subthalamic nucleus contributes to the synchronization process underlying the emergence of feelings.
- Inadequate use of acoustic features has a major impact on emotional judgments in patients with Parkinson’s disease, affecting the extraction and integration of acoustic cues during emotion perception.
- The basal ganglia are sensitive to rhythm because of their intrinsic functional role as organizer ‑ or coordinator ‑ of neural patterns.
- A right orbitofrontal‑basal ganglia coupling seems to be specifically involved in the vocal emotion recognition deficit observed in Parkinson’s disease. Its precise role remains to be elucidated.
EXAMPLES OF CLINICAL AND APPLIED IMPLICATIONS
- Both clinicians and individuals living with Parkinson’s disease should be aware of the potential adverse effects of subthalamic nucleus deep brain stimulation. Predictive factors for these disturbances are starting to be identified, but have yet to be fully explored.
- Stimulation electrodes are located the most dorsally possible, while directional electrodes are used to target the motor part of the structure in order to avoid cognitive or emotional adverse effects.
- The side of motor onset and the asymmetry of motor symptoms are important clinical factors, as they may influence the presence or severity of affective disorders in Parkinson’s disease.
- Dopatherapy may have a deleterious effect on affective abilities in the early stages of Parkinson’s disease (i.e., dopaminergic overdose effect).
- Neurorehabilitation is being developed for people living with neurological or psychiatric disorders. One aim is to restore basic sensory processes, in order to improve high-level cognitive evaluative judgements.