Roles for the Dorsal Striatum in Aversive Behavior

Abstract

The ability to identify and avoid environmental stimuli that signal danger is essential to survival. Our understanding of how the brain encodes aversive behaviors has been primarily focused on roles for the amygdala, hippocampus (HIPP), prefrontal cortex, ventral midbrain, and ventral striatum. Relatively little attention has been paid to contributions from the dorsal striatum (DS) to aversive learning, despite its well-established role in stimulus-response learning. Here, we review studies exploring the role of DS in aversive learning, including different roles for the dorsomedial and dorsolateral striatum in Pavlovian fear conditioning as well as innate and inhibitory avoidance (IA) behaviors. We outline how future investigation might determine specific contributions from DS subregions, cell types, and connections that contribute to aversive behavior.

Keywords: aversion; dorsal striatum; fear conditioning; inhibitory avoidance; threat.

Figure 1

The amygdala and dorsal striatum (DS) may be similarly positioned to influence fear learning. (A) The conventional circuit model of fear learning with a central role for the amygdala (in green). (B) A circuit model that places the (DS in orange) in a similar position to the amygdala in regulating fear conditioning. Note that the amygdala and DS share inputs from the sensory cortex (S) and medial prefrontal cortex (MPFC) which is important for connecting aversive events with sensory stimuli and that both circuits converge on periaqueductal gray (PAG, in red), which is critical for mediating freezing behavior. Basal lateral amygdala (BLA), central amygdala (CEA), substantia nigra reticulata (SNR), globus pallidus (GP), superior colliculus (SC), inferior colliculus (IC), hippocampus (HIPP), thalamus (THAL), limbic cortex (LC).

Figure 2

Evidence for DS’s role in aversive behavior. (A) The upper chart highlights studies that demonstrate a correlation between DS activity during different stages of cue fear conditioning. The lower chart highlights studies on the effect of DS manipulations on cue fear learning. (B) Studies examining the effect of context fear conditioning on DS activity (top) and the effect of DS manipulations on context fear learning (bottom). Central amygdala (CEA), medial geniculate nucleus (MGN), dorsal striatum (DS), dorsal medial striatum (DMS), dorsolateral striatum (DLS), the tail of the striatum (TS). (C) Evidence for DS’s role in inhibitory and innate avoidance. Dorsal striatum (DS), dorsal medial striatum (DMS), dorsolateral striatum (DLS), substantia nigra reticulata (SNR).