The role of the deeper layers of the superior colliculus in attentional modulations of prepulse inhibition

Abstract

Prepulse inhibition (PPI) is the suppression of the startle reflex, when a weaker non-startling sensory stimulus (the prepulse) precedes the intense startling stimulus. Although the basic PPI neural circuitry resides in the brainstem, PPI can be enhanced by selective attention to the prepulse, indicating that this sensorimotor-gating process is influenced by higher-order perceptual/cognitive processes. Along with the auditory cortex, the brain structures involved in attentional modulations of PPI include both the lateral nucleus of the amygdala (LA), which contributes to the fear-conditioning modulation, and the posterior parietal cortex (PPC), which contributes to the spatially attentional modulation. The deeper layers of the superior colliculus (DpSC), which has been suggested as a midbrain component in the PPI circuitry, receive descending axonal projections from some forebrain structures associated with auditory perception, emotional conditioning, or spatial attention. This study was to examine whether the DpSC are also involved in attentional modulations of PPI in rats. The results showed that both fear conditioning of a prepulse sound and precedence-effect-induced perceptual separation between the conditioned prepulse and a noise masker facilitated selective attention to the prepulse and consequently enhanced PPI. Reversibly blocking glutamate receptors in the DpSC with 2-mM kynurenic acid eliminated both the conditioning-induced and the perceptual-separation-induced PPI enhancements. However, the baseline magnitudes of startle and PPI were not affected. The results suggest that the DpSC play a role in mediating the attentional enhancements of PPI, probably through both receiving top-down signals from certain forebrain structures and modulating the midbrain representations of prepulse signals.

Keywords: Attentional modulation; Fear conditioning; Perceptual separation; Precedence effect; Prepulse inhibition; Startle reflex.