Evolving Concepts of Arousal: Insights from Simple Model Systems

Abstract

Arousal states strongly influence behavioral decisions. In general, arousal promotes activity and enhances responsiveness to sensory stimuli. Earlier work has emphasized general, or nonspecific, effects of arousal on multiple classes of behaviors. However, contemporary work indicates that arousal has quite specific effects on behavior. Here we review studies of arousal-related circuitry in molluscan model systems. Neural substrates for both general and specific effects of arousal have been identified. Based on the scope of their actions, we can distinguish two major classes of arousal elements: localized versus general. Actions of localized arousal elements are often limited to one class of behavior, and may thereby mediate specific effects of arousal. In contrast, general arousal elements may influence multiple classes of behaviors, and mediate both specific and nonspecific effects of arousal. One common way in which general arousal elements influence multiple behaviors is by acting on localized arousal elements of distinct networks. Often, effects on distinct networks have different time courses that may facilitate formation of specific behavioral sequences. This review highlights prominent roles of serotonergic systems in arousal that are conserved in gastropod molluscs despite extreme diversification of body forms, diet and ecological niches. The studies also indicate that the serotonergic elements can act as either localized or general arousal elements. We discuss the implications of these findings across animals.

Characterization of GdFFD, a d-Amino Acid-containing Neuropeptide That Functions as an Extrinsic Modulator of the Aplysia Feeding Circuit

“…We would like to emphasize that the choice of the feeding circuit for the study of circuit function of DAACPs is not random, because the expression of specific feeding behavior, which is a motivated behavior, is modulated by many intrinsic and extrinsic factors (36,76) that are often mediated by actions of neuromodulators (36,(77)(78)(79). Consistent with this complexity, previous work has shown that the feeding circuit is extensively modulated by neuromodulators, including neuropeptides that have been discovered in Aplysia (41,42,48,49,66,67,69).…”

“…In fact, to the best of our knowledge, no studies have examined the effects of DAACPs on a defined neural circuit, likely due to the limited information on well defined neural circuits in most species. Here, we describe approaches to overcome these two limitations using a well known model animal, the sea slug Aplysia californica (35)(36)(37).…”

Composite Modulatory Feedforward Loop Contributes to the Establishment of a Network State

“…Localization of neuromodulators to specific neurons made it possible to change the focus of research from studying overall actions of modulators on CPG networks to more specific studies of how neuromodulators may account for the actions of individual neurons that contain them (e.g., Harris-Warrick and Marder 1991;Jing and Weiss 2001;Jing et al 2007Jing et al -2009Koh et al 2003;Nusbaum and Beenhakker 2002;Sakurai and Katz 2009). Such studies are well illustrated by the actions of two modulatory pathways in Aplysia: one of which originates in the higher-order interneuron, CBI-3 Morgan et al 2002) and the other in the EN.…”

“…This is true both for simple invertebrate motor networks (Briggman and Kristan 2008;Getting 1989;Jing 2009;Jing and Weiss 2005;Jing et al 2009;Marder et al 2005;Nusbaum and Beenhakker 2002) and for vertebrate neural networks (Grillner 2006;Lieske et al 2000) including cortical networks (Haider and McCormick 2009;Yuste et al 2005). In part, distinct network outputs stem from combinatorial actions of a variety of neuromodulators that sculpt a specific functional pattern from the anatomical connectivity of the network.…”

Evolution of consciousness: Phylogeny, ontogeny, and emergence from general anesthesia

“…Creatures that could meet their basic homeostatic needs are the ones that survived; those that did not suffered extinction. The brain structures needed for generating arousal and primitive emotional responses are generally located in the brainstem, midbrain, and limbic system and are as old as the vertebrate radiation itself (54).…”