Motivation for reward drives adaptive behaviors whereas impairment of reward perception

Motivation for reward drives adaptive behaviors whereas impairment of reward perception and experience (anhedonia) can contribute to psychiatric diseases including depression and schizophrenia. stimulation. This chronic mPFC overactivity also stably suppresses natural reward-motivated behaviors and induces specific new brainwide functional interactions which predict the degree of anhedonia in individuals. These findings describe a mechanism by which mPFC modulates expression of reward-seeking behavior by regulating the dynamical interactions between specific distant subcortical regions. The drive to pursue and consume rewards is highly conserved across species (1). Subcortical neuromodulatory systems including midbrain dopaminergic projections play a central role in predicting and signaling the availability of rewards (2–5). Anhedonia represents a core symptom of depression but also characterizes other neuropsychiatric disorders including schizophrenia suggesting the possibility of shared neural substrates (6). Although the underlying cause of anhedonia remains unknown a number of hypotheses exist including cortically driven dysregulation of subcortical circuits (7–10). Imaging studies have detected elevated metabolic activity in the mPFC of human patients suffering from XLKD1 depression (11); this type of brain activity is correlated with anhedonic symptoms (12–16). In particular the subgenual cingulate gyrus of the medial prefrontal cortex (mPFC) is a therapeutic target for deep brain stimulation in Kinetin refractory depression and treatment has been associated with normalization of this localized hyperactivity alongside patient reports of renewed interest in rewarding aspects of life Kinetin (11 17 18 By combining optogenetics with functional magnetic resonance imaging (fMRI) we sought to test the hypothesis that the mPFC exerts causal top-down control over Kinetin the interaction of specific subcortical regions governing dopamine-driven reward behavior with important implications for anhedonia. Although human fMRI experiments have resolved activity patterns in distinct subregions of the brain that respond to reward anticipation and experience (19 20 the causal relationships between neuronal activity in reward-related circuits and brainwide blood oxygen level–dependent (BOLD) patterns have yet to be established. In optogenetic fMRI (ofMRI) light-responsive regulators of transmembrane ion conductance (21) are introduced into target cell populations and controlled by focal pulses of light to assess the causal impact of the targeted circuit elements on local and global fMRI responses. We developed and extended this technique to scanning of awake rats and included a number of optogenetic tools specifically suited to our experimental questions. We began by mapping the brainwide BOLD response to optogenetic stimulation of dopamine neurons in transgenic tyrosine hydroxylase driver (TH-Cre) rats using an excitatory channelrhodopsin (ChR2 His134→Arg134 hereafter referred to as ChR2). Next we tested effects of a similarly targeted inhibitory opsin the enhanced halorhodopsin (eNpHR3.0) (22). We hypothesized that such inhibition of dopamine neurons would reduce BOLD activity in downstream regions although it is unknown whether tonic dopamine levels would be sufficient to allow detection of a downward modulation in BOLD. Furthermore the expected direction of the BOLD response is a matter of debate given the functional heterogeneity of dopamine receptors. Finally we assessed the influence Kinetin of mPFC excitability over this subcortical dopaminergic reward signaling. Altered excitability in the mPFC has been correlated with anhedonic behaviors in human patients and mice (23) and there is a growing body of literature characterizing altered resting-state BOLD correlations in patients with psychiatric disease (24). Kinetin Nevertheless it is still unclear whether and to what extent local changes in prefrontal cortex activity might propagate to distant brain regions to modulate reward-related signals. To address these questions we used the stabilized step-function opsin (SSFO) a double-mutant excitatory ChR2 (Cys128→Ser128 Asp156→Ala156) engineered to have slow off-kinetics (rate of channel closure τoff ~ 30 min) (23). Upon activation Kinetin by blue light SSFO.