Stress and the Mesocorticolimbic Dopamine Systemsa

Roth, Robert H.; Tam, See‐Ying; Ida, Yoshishige; Yang, Jingxia; Deutch, Ariel Y.

doi:10.1111/j.1749-6632.1988.tb42102.x

Cited by 324 publications

(187 citation statements)

References 17 publications

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“…If these findings were correct, they would suggest that dopaminergic afferents might be providing a non-adaptive hyperinnervation of a subpopulation of GABAergic interneurons, perhaps ones that are intrinsically impaired in schizophrenia. Since dopamine appears to exert an inhibitory effect on cortical GABA cells (Retaux et al 1991), these findings would predict that an excessive release of dopamine under conditions of stress (Thierry et al 1976;Roth et al 1988) could lead to an impairment of GABAergic function and ultimately to a decompensation of the intrinsic circuitry in layer II of anterior cingulate cortex (Benes 1997).…”

Section: Postmortem Evidence For a Gaba Defect In Schizophreniamentioning

confidence: 99%

GABAergic Interneurons Implications for Understanding Schizophrenia and Bipolar Disorder

Beneš

Berretta

2001

Neuropsychopharmacology

997

643

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Neurons that express the compound, ␥ -aminobutyric acid (GABA), are broadly present throughout the central nervous system, although telencephalic structures, such as the cerebral cortex, show the most abundant quantities of this neurotransmitter (Jones 1987). In the discussion that follows, the anatomy and physiology of various types of GABAergic interneurons in the cortex and hippocampus will be discussed and related to recent postmortem studies implicating this transmitter system in the pathophysiology of schizophrenia and bi- 25 , NO . 1 polar disorder and their treatment with neuroleptic drugs (for more comprehensive reviews on cortical and hippocampal neurons see: Hof et al. 1993;Freund and Buzsaki 1996;Somogyi et al. 1998). NEUROBIOLOGY OF GABAERGIC INTERNEURONSBased on Golgi-impregnation studies, Ramon y Cajal provided the first descriptions of several different morphological subtypes of interneurons in the cerebral cortex and hippocampus (Ramon y Cajal 1893, 1911. In more recent years, it has been shown that, with some overlap, different morphological subtypes also have distinct distributions, connectivity, neurochemistry, and electrophysiological properties (for reviews see Hof et al. 1993;Freund and Buzsaki 1996). It is interesting to note that every segment of a pyramidal neuron, such as the soma, dendritic branches and spines, and the initial axonal segment, receives dense GABAergic synaptic innervation (O'Kusky and Colonnier 1982;Hendry et al. 1983;Houser et al. 1983; Beaulieu et al. 1992; for reviews see Jones 1993;Freund and Buzsaki 1996). Even more interestingly, each of these segments appears to be innervated by distinct GABAergic neuronal subtypes (see below).These differences strongly suggest that each of these subtypes plays a fundamentally different role in physiological and pathological mechanisms. In the discussion that follows, cortical interneurons will be described first, since our most basic understanding of GABAergic cells is derived from these populations. In more recent years, however, similar characterizations of interneurons in hippocampus have emerged. Although these cells show some striking similarities to their cortical counterparts, there are also some unique features that distinguish them. For this reason, interneurons in the hippocampus are discussed separately. Cortex Neuroanatomical Studies of Cortical Interneurons.Various types of GABAergic neurons can be categorized according to the type of synaptic profiles they are associated with, as this has direct implications for understanding the physiological role of these cells in cortical circuits. These categories are discussed below.A XO -S OMATIC I NHIBITORY S YNAPSES (B ASKET C ELLS ). The most commonly encountered interneurons ( Figure 1A) are multipolar in shape, i.e., they may have three or more primary dendritic branches emanating from their cell bodies, some having somata that are as large as those of pyramidal neurons (Jones and Hendry 1984). Using immunocytochemistry to localize the enzyme ). These cells also ...

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Section: Postmortem Evidence For a Gaba Defect In Schizophreniamentioning

confidence: 99%

GABAergic Interneurons Implications for Understanding Schizophrenia and Bipolar Disorder

Beneš

Berretta

2001

Neuropsychopharmacology

997

643

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“…These two regions are of particular interest because previous work demonstrates that DA terminals within the PFC and Acc display greater responsivity to salient stimuli relative to other cortical (eg cingulate cortex) and subcortical (eg striatum, hypothalamus) DA terminal fields (Dunn, 1988;Roth et al, 1988;Feenstra et al, 2000). Thus, given the apparent lack of sensitivity of Acc DA terminals to HCRT-1, it seems unlikely that HCRT-1 activates DA terminals within these other areas.…”

Section: Circuitry Underlying Selective Increase In Da Efflux By Hcrtmentioning

confidence: 99%

“…Importantly, these various terminal fields display differential sensitivity to environmental and pharmacological manipulations. In particular, DA terminals within the PFC display the greatest sensitivity to both appetitive and aversive (eg stress) conditions (Thierry et al, 1976;Dunn, 1988;Roth et al, 1988;Cenci et al, 1992). Under similar conditions, Acc DA terminals typically display reduced, and striatal terminals minimal, reactivity (Dunn, 1988;Abercrombie et al, 1989;Cenci et al, 1992).…”

Section: Introductionmentioning

confidence: 99%

Hypocretin/Orexin Selectively Increases Dopamine Efflux within the Prefrontal Cortex: Involvement of the Ventral Tegmental Area

Vittoz

Berridge

2005

Neuropsychopharmacol

172

114

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Hypocretins (HCRTs) modulate a variety of behavioral and physiological processes, in part via interactions with multiple ascending modulatory systems. Further, HCRT efferents from the lateral hypothalamus innervate midbrain dopamine (DA) nuclei, and DA cell bodies express HCRT receptors. Combined, these observations suggest that HCRT may influence behavioral state and/or statedependent processes via modulation of DA neurotransmission. The current studies used in vivo microdialysis in the unanesthetized rat to first characterize the effect of intracerebroventricular infusion of HCRT-1 (0.07, 0.7 nmol) on extracellular levels of DA within the prefrontal cortex (PFC) and nucleus accumbens (Acc). Electroencephalographic/electromyographic measures of sleep-wake state were collected along with select behavioral measures (eg locomotor activity, grooming). HCRT-1 dose-dependently increased PFC dialysate DA levels, and these increases were closely correlated with increases in time spent awake. In contrast, Acc DA levels were unaffected. Additional studies examined whether HCRT-1 acts directly within the ventral tegmental area (VTA) to selectively increase PFC DA efflux and modulate behavioral state. Unilateral infusion of HCRT-1 (0.1, 1.0 nmol) within the VTA increased PFC, but not Acc, DA levels. Importantly, intra-VTA infusion of HCRT-1 increased the time spent awake and grooming. Moreover, HCRT-induced increases in both time spent awake and time spent grooming were significantly correlated with post-infusion PFC DA levels. The current observations predict a prominent modulatory influence of HCRT on PFC-dependent cognitive and affective processes that results, in part, from actions within the VTA. Additionally, these observations suggest that the activation of VTA DA neurons contributes to the behavioral state-modulatory actions of HCRT.

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“…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 levels (Abercrombie et al 1989).…”

mentioning

confidence: 99%

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

Moore

Rose

Grace

2001

Neuropsychopharmacology

113

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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...

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Stress and the Mesocorticolimbic Dopamine Systemsa

Cited by 324 publications

References 17 publications

GABAergic Interneurons Implications for Understanding Schizophrenia and Bipolar Disorder

GABAergic Interneurons Implications for Understanding Schizophrenia and Bipolar Disorder

Hypocretin/Orexin Selectively Increases Dopamine Efflux within the Prefrontal Cortex: Involvement of the Ventral Tegmental Area

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

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