Water temperature determines neurochemical and behavioural responses to forced swim stress: Anin vivomicrodialysis and biotelemetry study in rats

Abstract

Forced swimming is a behavioural stress model increasingly used to investigate the neurocircuitry of stress responses. Although forced swim stress clearly is a psychological stressor (anxiety, panic), its physical aspects are often neglected. There are indications that behavioural and neurochemical responses to swim stress depend on the water temperature. Thus, we investigated the responsiveness of hippocampal serotonergic neurotransmission (important in the coordination of stress responses), and of behaviour and core body temperature to forced swimming at different water temperatures (19, 25 and 35 degrees C). In vivo microdialysis and biotelemetry in freely-behaving rats were used. Dialysates were analysed for serotonin (5-HT) and its metabolite 5-HIAA (5-hydroxyindoleacetic acid) by HPLC with electrochemical detection. Forced swimming in water at 25 and 19 degrees C decreased core body temperature by 8 and 12 degrees C, respectively. A rapid and pronounced increase in hippocampal 5-HT and 5-HIAA was found in rats that swam at 35 degrees C, whereas biphasic responses in 5-HT and 5-HIAA were observed at 25 and 19 degrees C. Also swim stress behaviour and post-stress home cage behaviour depended on the water temperature. Comparing the serotonergic and core body temperature changes revealed that a combination of two different 5-HT and 5-HIAA responses seems to shape the neurotransmitter response. Swimming-induced increases in hippocampal extracellular concentrations of 5-HT and 5-HIAA occurred at all water temperatures, but these increases were temporarily quenched, or concentrations were transistently decreased, when core body temperature fell below 31 degrees C in water at 25 or 19 degrees C. These data demonstrate that water temperature is a key factor determining the impact of forced swim stress on behaviour and neurochemistry, and underscore that changes in these parameters should be interpreted in the light of the autonomic responses induced by this stressor.

Intermittent and continuous swim stress-induced behavioral depression: sensitivity to norepinephrine- and serotonin-selective antidepressants

“…Water temperature-dependent changes in serotonergic activity were observed using in vivo microdialysis, in the hippocampus, during and up to 90 min post-swim using 19°C, 25°C, or 35°C water temperatures. Cold water exposure (19°C) blocked the increase in extracellular serotonin and 5-hydroxyindoleacetic acid (the main metabolite of serotonin) that was observed at the two higher temperatures (Linthorst et al 2008).…”

Hippocampal gene expression induced by cold swim stress depends on sex and handling

“…Therefore, it is likely that other peptide hormones or neurotransmitter systems -which respond specifically to the swim stress challenge -are involved in the strong and rapid regulation of Fos, Per1 and Sgk1. Possible neurotransmitter systems involved could be norepinephrine and serotonin, both of which are very strongly increased after cold swim stress (Gotoh et al, 1998;Linthorst et al, 2008), show sex-specific responses to stressful stimuli (Curtis et al, 2006;Pitychoutis et al, 2012), and can stimulate Fos expression (Castro et al, 2003;Gubits et al, 1989). In addition, glutamate may also be involved in the regulation of stress-induced gene expression, as NMDA-receptor antagonists have been shown to block the stress-induced increase in Fos expression in the hippocampus (Bozas et al, 1997).…”

That warm fuzzy feeling: brain serotonergic neurons and the regulation of emotion

“…Also consistent with the existence of a thermosensitive subpopulation of serotonergic neurons within the DRI, the water temperature used in the forced swim test (a test commonly used to detect antidepressant-like properties of drugs) determines the amount of serotonin release in the hippocampus, a main target of DRI serotonergic neurons (Köhler and Steinbusch, 1982;Linthorst, et al, 2007). In this test, higher temperatures result in greater serotonin release in the hippocampus, as would be expected if a subset of serotonergic neurons projecting to the hippocampus was temperature sensitive.…”