The activity of isolated snail neurons controlling locomotion is affected by glucose

Abstract

The involvement of serotonin in mediating hunger-related changes in behavioral state has been described in many invertebrates. However, the mechanisms by which hunger signals to serotonergic cells remain unknown. We tested the hypothesis that serotonergic neurons can directly sense the concentration of glucose, a metabolic indicator of nutritional state. In the snail Lymnaea stagnalis, we demonstrate that completely isolated pedal serotonergic neurons that control locomotion changed their biophysical characteristics in response to glucose application by lowering membrane potential and decreasing the firing rate. Additionally, the excitatory response of the isolated serotonergic neurons to the neuroactive microenvironment of the pedal ganglia was significantly lowered by glucose application. Because hunger has been reported to increase the activity of select neurons and their responses to the pedal ganglia microenvironment, these responses to glucose are in accordance with the hypothesis that direct glucose signaling is involved in the mediation of the hunger-related behavioral state.

Serotonin in Animal Cognition and Behavior

“…5-HT is a major neuromodulator of motor behaviors ( Figure 1A) in many species belonging to different invertebrate phyla. This includes flatworms [58], cnidarians [59], nematodes [60], annelids [61,62], arthropods (insects and crustaceans, [63][64][65]), and mollusks [66][67][68][69]. Part of our knowledge comes from studies investigating the ecological/toxicological consequences of SSRIs used as antidepressants, released in sanitary water, and finally spread in rivers [63,65,[70][71][72].…”

Snails prefer it sweet: A multifactorial test of the metal defence hypothesis

“…A, B). Interestingly, experiments with snail serotonergic neurons have shown that glucose is involved in the signalling of hunger to these neurons that control locomotion (Dyakonova et al ). Our snails had been starved for 7 days before the experimental feeding; thus, the glucose concentration in the offered plants may have acted as a potent feeding stimulant.…”

Responses of Withdrawal Interneurons to Serotonin Applications in Naïve and Learned Snails Are Different

“…Recently, the importance of extrasynaptic serotonergic transmission in memory has been recognized (Ierusalimskii and Balaban, 2010 ; Sakharov, 2012 ; Hirayama et al, 2014 ). Research by D. A. Sakharov showed that dynamic fluctuations of levels of monoamines (primarily 5-HT in mollusks) in the local extracellular environment can determine the physiological properties and receptor profiles of individual neurons and the character of their self-organization into a pattern-generating ensemble (Sakharov, 1990 , 2012 ; Dyakonova et al, 2015 ).…”

“…Serotonin (5-HT) is a major neuromodulator for the nervous system of mollusks. It has been found that 5-HT is the main transmitter that modulates the withdrawal behavior in mollusks and it is necessary for the associative memory formation (Kandel and Schwartz, 1982 ; Balaban et al, 1987 ; Gainutdinov et al, 1999 ; Pavlova, 2001 ; Burrell and Sahley, 2005 ; D’iakonova, 2007 ; Il-Han et al, 2010 ; Hirayama et al, 2014 ; Dyakonova et al, 2015 ). Recently (Ierusalimskii and Balaban, 2010 ; Sakharov, 2012 ) the concept concerning that the volume (extra-synaptic) transmission of 5-HT plays a major role in the mechanisms of memory in mollusks was discussed.…”