Stimulation of subterritories of the subthalamic nucleus reveals its role in the integration of the emotional and motor aspects of behavior

Abstract

Two parkinsonian patients who experienced transient hypomanic states when the subthalamic nucleus (STN) was stimulated during postoperative adjustment of the electrical parameters for antiparkinsonian therapy agreed to have the mood disorder reproduced, in conjunction with motor, cognitive, and behavioral evaluations and concomitant functional neuroimaging. During the experiment, STN stimulation again induced a hypomanic state concomitant with activation of cortical and thalamic regions known to process limbic and associative information. This observation suggests that the STN plays a role in the control of a complex behavior that includes emotional as well as cognitive and motor components. The localization of the four contacts of the quadripolar electrode was determined precisely with an interactive brain atlas. The results showed that (i) the hypomanic state was caused only by stimulation through one contact localized in the anteromedial STN; (ii) both this contact and the contact immediately dorsal to it improved the parkinsonian motor state; (iii) the most dorsal and ventral contacts, located at the boundaries of the STN, neither induced the behavioral disorder nor improved motor performance. Detailed analysis of these data led us to consider a model in which the three functional modalities, emotional, cognitive, and motor, are not processed in a segregated manner but can be subtly combined in the small volume of the STN. This nucleus would thus serve as a nexus that integrates the motor, cognitive, and emotional components of behavior and might consequently be an effective target for the treatment of behavioral disorders that combine emotional, cognitive, and motor impairment.basal ganglia ͉ emotion ͉ deep brain stimulation ͉ neuroimaging

Response inhibition rapidly increases single-neuron responses in the subthalamic nucleus of patients with Parkinson's disease

“…Therefore, we speculate that the absence of error-monitoring cells in PD might be related to a lower sampling of the STN subregions where these cells might be clustered. This idea would support a tripartite model of STN functional subterritories, in coherence with previous neuroimaging (Haynes & Haber, 2013;Karachi et al, 2005;Parent, 1990) and stimulation studies Lambert et al, 2011;Mallet et al, 2007;Sudhyadhom et al, 2007).…”

Deep brain stimulation in Parkinson disease—what went wrong?

“…Case reports of PD patients with reversible changes in behaviour related to an acute increase in stimulation parameters comprise mirthful laughter [50], pathological crying [51], mania [25,52,53], aggressive behaviour [54] and acute dysphoria or depression [55,56]. Furthermore, STN DBS can contribute to certain impulsive behaviours during high-conflict decisions [57].…”

Changes of oscillatory activity in the subthalamic nucleus during obsessive-compulsive disorder symptoms: Two case reports

“…Recently it has been shown that severe refractory OCD symptoms can be improved by high frequency stimulation of the subthalamic nucleus (STN) (Chabardè s et al, 2012;Fontaine et al, 2004;Mallet et al, 2008). The STN is a key * Corresponding author.…”

“…Recently it has been shown that severe refractory OCD symptoms can be improved by high frequency stimulation of the subthalamic nucleus (STN) (Chabardè s et al, 2012;Fontaine et al, 2004;Mallet et al, 2008). The STN is a key structure of basal ganglia connecting motor, limbic and associative systems, because it is known from Parkinson's disease (PD) patients that deep brain stimulation (DBS) of the STN can have significant effects on mood and cognition, including mirthful laughter (Krack et al, 2001), acute depression (Bejjani et al, 1999), aggressiveness (Bejjani et al, 2002), hypomania or full blown mania (Krack et al, 2001;Mallet et al, 2007;Ulla et al, 2011).…”

“…The STN is a key structure of basal ganglia connecting motor, limbic and associative systems, because it is known from Parkinson's disease (PD) patients that deep brain stimulation (DBS) of the STN can have significant effects on mood and cognition, including mirthful laughter (Krack et al, 2001), acute depression (Bejjani et al, 1999), aggressiveness (Bejjani et al, 2002), hypomania or full blown mania (Krack et al, 2001;Mallet et al, 2007;Ulla et al, 2011). Those transient effects are usually seen as "side effects" in PD, but are clues to the heretoforeunderappreciated role that STN plays in limbic circuitry, whose precise functions are as yet unknown and under active investigation (Buot et al, 2012;Kü hn et al, 2005;Pé ron, Frü hholz, Vé rin, & Grandjean, 2013).…”