Chronic Cold Stress Reduces the Spontaneous Activity of Ventral Tegmental Dopamine Neurons

Abstract

The dopamine (DA) Stress-induced changes in forebrain dopamine (DA) transmission have been implicated in the symptomatology of a number of psychiatric disorders including schizophrenia (Grace 1991; Seeman et al. 1976), major depression (Anisman and Zacharko 1990;Willner 1995), and behavioral disorders related to drug abuse (Quick et al. 1986). The mesoaccumbens and mesocortical DA systems, comprised of cells in the ventral tegmental area (VTA) and medial substantia nigra pars compacta (mSN) projecting to the medial prefrontal cortex (mPFC) or nucleus accumbens (NAc; Fallon and Loughlin 1995), have been shown to be sensitive to a number of stressors (Horger and Roth 1996). For example, multiple studies have shown that rodents exposed acutely to a stressor such as tail shock, foot shock or restraint exhibit marked increases in extracellular DA levels in the mPFC and moderate increases in the NAc and/or striatum (Abercrombie et al. 1989;Roth et al. 1988;Thierry et al. 1976; for review, see Finlay and Zigmond 1997). Moreover, whereas mild stressors fail to increase DA levels in the NAc and dorsal striatum, they can evoke significant increases in prefrontal cortical DA (Herman et al. 1982; cf. Horger and Roth 1996;Tissari et al. 1979).Thus, it appears that the DA projections from the VTA and substantia nigra are systematically activated during acute stress, with the sensitivity to stress being highest in the mesocortical DA system. Although the changes in mesoaccumbens and mesocortical DA transmission following acute exposure to a stressor have been well characterized, less is known about the response of these systems to chronic stress or exposure to highly traumatic conditions. However, there is evidence that DA release in the NAc and PFC may show some adaptation to the stressor after repeated (Cabib and Puglisi-Allegra 1996;Imperato et al. 1992Imperato et al. , 1993 or chronic (Gresch et al. 1994;Mizoguchi et al. 2000) exposure. Finlay et al. (1995) have shown that following chronic exposure to inescapable cold, considered a chronic stressor, extracellular DA levels in the NAc and PFC are unchanged or slightly lower than in controls (Gresch et al. 1994). Moreover, examined across studies, DA efflux evoked by a novel stressor appears to be similar in cold-stressed and control rats (Finlay et al. 1995;Gresch et al. 1994). Thus, it appears that in contrast to their responses to acute stress, the mesocortical and mesolimbic DA systems may show adaptation in response to chronic stress (see also Ortiz et al. 1996). The DAergic response contrasts with the sensitization of the sympathetic innervation to the adrenals and heightened response of the NE-containing neurons of the locus coeruleus in cold-stressed rats (Finlay et al. 1995;Fluharty et al. 1985;Gresch et al. 1994;Jedema et al. 1999Jedema et al. , 2001Mana and Grace 1997). This potentially distinct response of midbrain DA neurons to chronic stress may be relevant to the anhedonia and psychomotor slowing associated with post-traumatic stress disorder (Yehuda and A...

Influence of Phasic and Tonic Dopamine Release on Receptor Activation

“…It is thus possible that firing patterns composed of bursts followed by pauses mediate a different signal than isolated bursts associated with rewards. This is in accord with observations of increased burst firing with stressful stimuli (Moore et al, 2001;Anstrom and Woodward, 2005;Anstrom et al, 2009). In this context, our results indicate that the important signal in "spontaneous burst firing" may be the pauses between bursts.…”

“…However, dopamine neurons are characterized by a continuum of firing patterns from regular pacemaker firing to burst firing (Hyland et al, 2002). Typical firing patterns may have 50% spikes in bursts (Moore et al, 2001;Floresco et al, 2003). We therefore asked whether the observed modulation of ͳD 2 ʹ also applies for more realistic spike trains.…”

Increased perceived stress is associated with blunted hedonic capacity: Potential implications for depression research

“…In animals, chronic stressors have been found to impact the mesocorticolimbic dopamine pathways implicated in reward processing (Wise, 2004;Schultz, 2002) and induce anhedonic-like symptoms (Cabib & PuglisiAllegra, 1996;Moore, Rose, & Grace, 2001). Of relevance to the present study, this animal research suggests that stressor controllability is an important factor influencing the relationship between stress, dopamine, and hedonic behavior.…”

Postpartum and Depression Status are Associated With Lower [11C]raclopride BPND in Reproductive-Age Women

“…Although the current study cannot clarify whether lower D 2/3 receptor binding is a mechanism or consequence of postpartum status or depression, it is noteworthy that animal models of depression and chronic stress similarly revealed lower D 2/3 receptor mRNA in ventral striatum in rodents (Dziedzicka-Wasylewska et al, 1997) and lower [ 11 C]raclopride-PET measurements in nonhuman primates (Morgan et al, 2002;Shively et al, 1997). In rodents, chronic (Moore et al, 2001) and acute (Valenti et al, 2011) stressors were associated with increased subpopulations or total DA neuron burst firing. On this basis, in depressed and postpartum subjects in this cohort, the combination of chronic (depression or childcare stress) and acute stress (arterial cannulation/PET scanning procedure; Drevets et al, 2002) could also conceivably increase phasic DA release that could compete with [ 11 C]raclopride binding.…”