A Neuronal Network Switch for Approach/Avoidance Toggled by Appetitive State

Abstract

Summary Concrete examples of computation and implementation of cost-benefit decisions at the level of neuronal circuits are largely lacking. Such decisions are based on appetitive state, which is the integration of sensation, internal state and memory. Value-based decisions are accessible in neuronal circuitry of simple systems [1]. In one such, the predatory sea-slug Pleurobranchaea, appetite is readily quantified in behavior [2] and related to approach-avoidance decision [3]. Moreover, motor aspects of feeding and turning can be observed as fictive motor output in the isolated CNS [4,5]. Here we found that the excitation state of the feeding motor network both manifested appetitive state and controlled expression of orienting vs. avoidance. In isolated CNS’s spontaneous feeding network activity varied proportionally to donor feeding thresholds. CNS’s from low and high feeding threshold donors expressed fictive orienting or avoidance, respectively, in response to brief stimulation of sensory nerves. Artificially exciting the feeding network converted fictive avoidance to orienting. Thus, the feeding network embodied appetitive state and toggled approach-avoidance decision by configuring response symmetry of the premotor turn network. A resulting model suggests a basic cost-benefit decision module from which to consider evolutionary elaboration of the circuitry to serve more intricate valuation processes in complex animals.

The Activity of Isolated Neurons and the Modulatory State of an Isolated Nervous System Represent a Recent Behavioural State

“…The storage of the nutritional state in an isolated nervous system has been demonstrated earlier in Lymnaea (Elliott and Andrew, 1991;Hernádi et al, 2004) and other molluscs (Gillette, 2006;Hirayama and Gillette, 2012;Hirayama et al, 2014). The results of the present study agree with these previous studies and show that 24-36 h of food deprivation causes an excitation of CGC and PeA serotonergic neurons in intact ganglia (isolated CNS).…”

“…The role of serotonin in mediating a hunger/feeding behavioural state has been suggested and proved in many invertebrates (Horvitz et al, 1982;Lent and Dickinson, 1988;Sakharov, 1990a;Sakharov, 1990b;Palmer and Kristan, 2011;Donnelly et al, 2013), including molluscs (Alania et al, 2004;Hernádi et al, 2004;Gillette, 2006;Hirayama and Gillette, 2012;Hirayama et al, 2014;Dyakonova, 2014). In this study, we utilized the advantages of the mollusc Lymnaea stagnalis to elucidate how a hunger behavioural state is represented at a single serotonergic cellular level.…”

Implementing Goal-Directed Foraging Decisions of a Simpler Nervous System in Simulation

“…It defines the thresholds for decisions to approach or avoid given prey items. It parallels expression of appetitive state in the excitation of Pleurobranchaea ’s feeding network (Hirayama and Gillette, 2012). The sigmoidal element increases App_State as Incentive increases and decreases it as Satiation increases.…”

“…The neuronal circuitry of decision has been characterized down to the single-neuron level (Gillette et al, 1982; London and Gillette, 1986; Jing and Gillette, 2000, 2003; Hirayama and Gillette, 2012; Hirayama et al, 2012, 2014). In particular, a key decision mechanism was found to lie in regulation of the turn motor network by the feeding network, whose excitation state depends on sensory input, memory, and satiation.…”

“…In particular, a key decision mechanism was found to lie in regulation of the turn motor network by the feeding network, whose excitation state depends on sensory input, memory, and satiation. Sufficient excitation in the feeding network converts default avoidance responses to sensory stimuli to approaching turns (Hirayama and Gillette, 2012). These findings localized motivation, appetitive state, and control of motor decision to the feeding network.…”