Serotonergic Modulation of Plasticity of the Auditory Cortex Elicited by Fear Conditioning

Abstract

In the awake big brown bat, 30 min auditory fear conditioning elicits conditioned heart rate decrease and long-term best frequency (BF) shifts of cortical auditory neurons toward the frequency of the conditioned tone; 15 min conditioning elicits subthreshold cortical BF shifts that can be augmented by acetylcholine. The fear conditioning causes stress and an increase in the cortical serotonin (5-HT) level. Serotonergic neurons in the raphe nuclei associated with stress and fear project to the cerebral cortex and cholinergic basal forebrain. Recently, it has been shown that 5-HT 2A receptors are mostly expressed on pyramidal neurons and their activation improves learning and memory. We applied 5-HT, an agonist (␣-methyl-5-HT), or an antagonist (ritanserin) of 5-HT 2A receptors to the primary auditory cortex and discovered the following drug effects: (1) 5-HT had no effect on the conditioned heart rate change, although it reduced the auditory responses; (2) 4 mM 5-HT augmented the subthreshold BF shifts, whereas 20 mM 5-HT did not; (3) 20 mM 5-HT reduced the long-term BF shifts and changed them into short-term; (4) ␣-methyl-5-HT increased the auditory responses and augmented the subthreshold BF shifts as well as the long-term BF shifts; (5) in contrast, ritanserin reduced the auditory responses and reversed the direction of the BF shifts. Our data indicate that the BF shift can be modulated by serotonergic neurons that augment or reduce the BF shift or even reverse the direction of the BF shift. Therefore, not only the cholinergic system, but also the serotonergic system, plays an important role in cortical plasticity according to behavioral demands.

Context-dependent fluctuation of serotonin in the auditory midbrain: the influence of sex, reproductive state, and experience

“…These findings suggest that the serotonergic system is able to draw on information about both internal state and behavioral context in order to influence auditory processing on a time scale matched to behavior. Given that the serotonergic system is known to modulate auditory processing, it is an excellent system in which to measure the neurochemical mediation of context on sensory processing (Ebert and Ostwald, 1992;Hurley et al, 2002;Hurley and Pollak, 2005;Ji and Suga, 2007).…”

The role of serotonin in the enhancement of long-term memory resulting from predator detection in Lymnaea

“…In particular, stressrelated behavioural arousal and vigilance are known to be modulated by a serotonergic system in mammals (Amat et al, 1998b;Amat et al, 1998c). Serotonin is thought to be involved in the process of memory consolidation following one-trial avoidance and fear conditioning which often elicits an increase in anxiety (Inoue et al, 1993;Inoue et al, 1994;Izquierdo et al, 2006;Ji and Suga, 2007;Ogren et al, 2008). Studies investigating the effect of stress on longterm potentiation (LTP) have also indicated that a serotonergic system has a variety of modulatory effects on LTP depending on the learning events (e.g.…”

Corticofugal Modulation of Initial Sound Processing in the Brain

“…There are six hierarchical information processing levels in the central auditory system. The highest level is the auditory cortex where the learned or experienced sounds are registered (Edeline et al, 1993;Recanzone et al, 1993;Bakin and Weinberger, 1996;Pantev et al, 1998;Zhang et al, 2001Zhang et al, , 2006Ma and Suga, 2003;Polley et al, 2006;Alain et al, 2007;Froemke et al, 2007;Ji and Suga, 2007). The lowest level is the cochlear nucleus (CN) that gates all incoming signals from the ear to the brain (Kiang et al, 1967;Evans, 1975;Liberman and Kiang, 1978;Feng and Vater, 1985;Taberner and Liberman, 2005).…”