Abstract
Approach or avoidance behaviors are accompanied by perceptual vigilance for, affective reactivity to and behavioral predisposition towards rewarding or punitive stimuli, respectively. We detected three subpopulations of C57BL/6J mice that responded with avoiding, balancing or approaching behaviors not induced by any experimental manipulation but spontaneously displayed in an approach/avoidance conflict task. Although the detailed neuronal mechanisms underlying the balancing between approach and avoidance are not fully clarified, there is growing evidence that endocannabinoid system (ECS) plays a critical role in the control of these balancing actions. The sensitivity of dorsal striatal synapses to the activation of cannabinoid CB1 receptors was investigated in the subpopulations of spontaneously avoiding, balancing or approaching mice. Avoiding animals displayed decreased control of CB1 receptors on GABAergic striatal transmission and in parallel increase of behavioral inhibition. Conversely, approaching animals exhibited increased control of CB1 receptors and in parallel increase of explorative behavior. Balancing animals reacted with balanced responses between approach and avoidance patterns. Treating avoiding animals with URB597 (fatty acid amide hydrolase inhibitor) or approaching animals with AM251 (CB1 receptor inverse agonist) reverted their respective behavioral and electrophysiological patterns. Therefore, enhanced or reduced CB1-mediated control on dorsal striatal transmission represents the synaptic hallmark of the approach or avoidance behavior, respectively. Thus, the opposite spontaneous responses to conflicting stimuli are modulated by a different involvement of endocannabinoid signaling of dorsal striatal neurons in the range of temperamental traits related to individual differences.
Highlights
The super-ordinate division of emotions is distributed along a bipolar dimension of affective valence, from approaching to avoiding stimuli [1,2]
A/A Y-Maze In both Session 1 (S1) and Session 2 (S2), the choices of 206 animals fitted the normal distribution fairly well. When both arms were rewarded with the same standard food (S1), most entries the animals made were in the reassuring black arm (1360 black choices versus 700 white choices out of 2060 total entries)
When the aversive white arm was rewarded with the palatable food (S2), the distribution curve shifted towards the white choices (921 white choices out of 2060 total entries) (Fig. 1A)
Summary
The super-ordinate division of emotions is distributed along a bipolar dimension of affective valence, from approaching to avoiding stimuli [1,2]. Cocaine-induced conditioned place preference as well as running wheel spontaneous activity or sucrose consumption (manipulations with strong rewarding and reinforcing properties) are associated with hypersensitivity of striatal GABAergic synapses to CB1 receptors stimulation [25,26]. These findings raise the intriguing possibility that even spontaneous forms of reward-based behaviors may rely on the sensitization of CB1 receptor-mediated GABAergic transmission in the striatum. Given we were searching for individual differences in a spontaneous behavior not induced by any experimental manipulation, the behavior of adolescent mice in a conflict task able to reveal temperamental traits of approach or avoidance was analyzed. The spontaneous behavior of mice submitted to an approach/avoidance conflict task and the CB1mediated transmission in spiny neurons of the dorso-medial striatum, structure crucially involved in motivated and goaldirected behaviors [34,35,36,37], were analyzed
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