Physical (exteroceptive) stimuli and emotional (interoceptive) stimuli are thought to influence stress-related physiologic and behavioral responses through different neural mechanisms. Previous studies have demonstrated that stress-induced activation of brainstem serotonergic systems is influenced by environmental factors such as temperature. In order to further investigate the effects of environmental influences on stress-induced activation of serotonergic systems, we exposed adult male Wistar rats to either home cage control conditions or a 15 min swim in water maintained at 19 °C, 25 °C, or 35 °C and conducted dual immunohistochemical staining for c-Fos, a marker of immediate-early nuclear activation, and tryptophan hydroxylase (TPH), a marker of serotonergic neurons. Changes in core body temperature were documented using biotelemetry. As expected, exposure to cold (19 °C) swim, relative to warm (35 °C) swim, increased c-Fos expression in the external lateral part of the parabrachial nucleus (LPBel), an important part of the spinoparabrachial pathway involved in sensation of cold, cutaneous stimuli, and in serotonergic neurons in the raphe pallidus nucleus (RPa), an important part of the efferent mechanisms controlling thermoregulatory warming responses. In addition, exposure to cold (19 °C) swim, relative to 35 °C swim, increased c-Fos expression in the dorsal raphe nucleus, ventrolateral part/periaqueductal gray (DRVL/VLPAG) and dorsal raphe nucleus, interfascicular part (DRI). Both of these subregions of the dorsal raphe nucleus (DR) have previously been implicated in thermoregulatory responses. Altogether, the data are consistent with the hypothesis that midbrain serotonergic neurons, possibly via activation of afferents to the DR by thermosensitive spinoparabrachial pathways, play a role in integration of physiologic and behavioral responses to interoceptive stress-related cues involved in forced swimming and exteroceptive cues related to cold ambient temperature.

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Prior adverse experience alters behavioral responses to subsequent stressors. For example, exposure to a brief swim increases immobility in a subsequent swim test 24 h later. In order to determine if qualitative differences (e.g. 19 °C versus 25 °C) in an initial stressor (15 min swim) impact behavioral, physiological, and associated neural responses in a 5 min, 25 °C swim test 24 h later, rats were surgically implanted with biotelemetry devices one week prior to experimentation then randomly assigned to one of 6 conditions (Day 1 (15 min)/Day 2 (5 min)): 1) home cage (HC)/HC, 2) HC/25 °C swim, 3) 19 °C swim/HC, 4) 19 °C swim/25 °C swim, 5) 25 °C swim/HC, 6) 25 °C swim/25 °C swim. Core body temperature (Tb) was measured on Days 1 and 2 using biotelemetry; behavior was measured on Day 2. Rats were transcardially perfused with fixative 2 h following the onset of the swim on Day 2 for analysis of c-Fos expression in midbrain serotonergic neurons. Cold water (19 °C) swim on Day 1 reduced Tb, compared to both 25 °C swim and HC groups on Day 1, and, relative to rats exposed to HC conditions on Day 1, reduced the hypothermic response to the 25 °C swim on Day 2. The 19 °C swim on Day 1, relative to HC exposure on Day 1, increased immobility during the 5 min swim on Day 2. Also, 19 °C swim, relative to HC conditions, on Day 1 reduced swim (25 °C)-induced increases in c-Fos expression in serotonergic neurons within the dorsal (DRD) and interfascicular (DRI) parts of the dorsal raphe nucleus (DR). These results suggest that exposure to a 5 min 19 °C cold water swim, but not exposure to a 5 min 25 °C swim alters physiological, behavioral and serotonergic responses to a subsequent stressor.

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