The Basolateral Amygdala and Superior Colliculus Regulate Physiological and Behavioral Measures of Avoidance and Approach

Abstract

The superior colliculus (SC) and amygdala are central components of the defensive system within the brain. The SC processes conscious and non-conscious visual information and directs orienting and defensive behavioral responses. The amygdala exerts “top down” control over SC and may interact with the SC to regulate emotional response to visual stimuli.

To determine the anatomical connectivity between the SC and the amygdala, I injected retrograde tracers into the amygdala and anterograde tracers into the SC and examined regions of colocalization within the pulvinar, a vision associated region. Anterograde tracers labeled axonal projections that colocalized with cell bodies labeled by the retrograde tracer, concentrated in the medial portions of the medial (PM), oral (PO) and inferior pulvinar (PI). These data support the existence of a "bottom up” pathway mediating fast processing of emotionally salient information projecting from the SC to the amygdala through the pulvinar.

To determine the causal association of activity in the amygdala on (1) autonomic activity, (2) emotional reactivity to social and threatening stimuli, and (3) social dominance, I used a pharmacological microinjection approach. I inhibited the amygdala via GABAA agonist muscimol (MUS) and activated it with GABAA antagonist bicuculline methiodide (BMI). Saline was injected as a control. Following drug infusion, animals were tested in the above behavioral domains. Activity in the amygdala was associated with decreased heart rate, nonspecific avoidance behavior, and decreased dominance. Inhibition of the amygdala was associated with decreased heart rate, reduced responsiveness to a threatening stimulus, increased responsiveness to a social stimulus, and decreased dominance.

To determine if activity within the SC regulated autonomic responses, I microinjected BMI into the SC and measured heart rate and blood pressure. Consistent with its laminar structure and segregated zones of anatomical inputs and outputs, subregions of the SC showed a diversity of responses, but primarily decreased heart rate and blood pressure, localized in intermediate and deep layers.

I have shown that BLA and SC separably regulate autonomic outputs. BLA additionally regulates behavioral response to threats and challenges to established behavioral patterns, reflecting alterations in larger networks involved in recognizing and responding appropriately to environmental cues.