State-Dependent Modulation of a Theta-Responsive Subnetwork by High-Frequency Stimulation of the Ventral Striatum
Wenlei Zhang1 · Xiaotian Wu1 · Chengjie Tang1 · Weicong Sang1 · Yujian Ye1 · Hong Gan1,2 · Tianzhen Chen1 · Ti‑Fei Yuan1,3 · Rongwei Zhai4 · Haifeng Jiang1 · Zhi‑Qi Xiong5 · Min Zhao1
1 Shanghai Mental Health Center, Shanghai Jiao Tong University School of Medicine, Shanghai 200030, China
2 Suzhou Guangji Hospital, The Affiliated Guangji Hospital of Soochow University, Suzhou 215008, China
3 School of Medicine and School of Psychology, Shanghai Jiao Tong University, Shanghai 200030, China
4 Hainan Academy of Medical Sciences, Hainan Medical University, Haikou 571199, China
5 CAS Center for Excellence in Brain Science and Intelligence Technology (CEBSIT), Chinese Academy of Sciences, Shanghai 200031, China
Abstract
The ventral striatum (VS) is a promising target for deep brain stimulation (DBS) for the treatment of refractory psychiatric disorders. The therapeutic effects of DBS rely on altering neural activity within specific networks; however, the network-level oscillatory mechanisms underlying VS-DBS remain unclear. Here, in human subjects with DBS electrodes implanted in the VS and anterior limb of the internal capsule, electroencephalography recordings obtained during DBS ON and OFF conditions revealed a global suppression of theta activity. To isolate these effects specific to VS stimulation, we applied direct electrical stimulation to the VS in two rhesus monkeys while simultaneously recording intracranial local field potentials from the reward-network regions. High-frequency stimulation (HFS) of the VS elicited target-specific, current-dependent, state-dependent, and distributed modulation of theta activity, whose magnitude was related to effective connectivity. Overall, VS-HFS exerted state-dependent modulation of a theta-responsive subnetwork. These findings may help to elucidate the therapeutic mechanisms of VS-DBS.
Keywords
Ventral striatum; Deep brain stimulation; State-dependent modulation; Reward network; Theta oscillations