Elsevier

Neuroscience

Volume 72, Issue 1, May 1996, Pages 141-156
Neuroscience

Burst stimulation of the medial forebrain bundle selectively increases Fos-like immunoreactivity in the limbic forebrain of the rat

https://doi.org/10.1016/0306-4522(95)00513-7Get rights and content

Abstract

The present study was designed to evaluate the postsynaptic functional consequences of different presynaptic activity patterns in midbrain dopamine systems using electrical stimulation of the rat medial forebrain bundle and subsequent determination of c-fos expression, used as a marker for neuronal activation, in dopamine target areas, by means of Fos immunohistochemistry. Nerve terminal dopamine release evoked by electrical stimulation of the medial forebrain bundle was monitored in the same animals usingin vivo voltammetry. A 5 Hz stimulation consisting of 60 trains of five pulses and lasting 1 min was applied to the medial forebrain bundle. This stimulation was repeated 15 times every 3 min. Its pattern was defined by the interpulse interval which was either 70 ms or 200 ms for burst or regularly spaced stimulation, respectively. Our results show that burst stimulation of the medial forebrain bundle, which increases release of dopamine in target areas, increases the basal Fos-like immunoreactivity in the stimulated hemisphere, while regular stimulation does not affect expression of this protein. Moreover, the increase in Fos-like immunoreactivity induced by burst stimulation is restricted to limbic related structures, i.e. nucleus accumbens shell and intermediate aspect of the lateral septum, and the major island of Calleja, but is not observed in motor related structures (nucleus accumbens core and striatum). Pretreatment with the D1 dopamine receptor antagonist, SCH23390 (0.1 mg/kg, i.p.), blocked the increase in Fos-like immunoreactivity induced by burst stimulation of the medial forebrain bundle, suggesting a role for these receptors in the observed effects. Pretreatment with the 5-hydroxytryptamine2A/2C receptor antagonist ritanserin (0.4 mg/kg, i.p.) did not affect the increase in Fos-like immunoreactivity induced by burst stimulation in the nucleus accumbens shell or in the lateral septum, although it blocked the stimulated enhancement of Fos-like immunoreactivity in the major island of Calleja.

The present data indicate that, rather than the absolute mean discharge rate of midbrain dopamine neurons, the temporal organization of the action potentials they generate conveys information to their target areas.

Reference (112)

  • DeutchA.Y. et al.

    Regionally specific effects of atypical antipsychotic drugs on striatal Fos expression: the nucleus accumbens shell as a locus of antipsychotic action

    Molec. cell. Neurosci.

    (1992)
  • Di ChiaraG. et al.

    Stimulation of dopamine transmission in the dorsal caudate nucleus by pargyline as demonstrated by dopamine and acetylcholine microdialysis and Fos immunohistochemistry

    Neuroscience

    (1993)
  • DragunowM. et al.

    D2 dopamine receptor antagonists induce Fos and related proteins in rat striatal neurons

    Neuroscience

    (1990)
  • FallonJ.H.

    The islands of Calleja complex of rat basal forebrain II: connections of medium and large sized cells

    Brain Res. Bull.

    (1983)
  • FreemanA.S. et al.

    Firing properties of substantia nigra dopaminergic neurons in freely moving rats

    Life Sci.

    (1985)
  • GarianoR.F. et al.

    Burst firing induced in midbrain dopamine neurons by stimulation of the medial prefrontal and anterior cingulate cortices

    Brain Res.

    (1988)
  • GononF.

    Non linear relationship between impulse flow and dopamine released by rat midbrain dopaminergic neurons as studied byin vivo electrochemistry

    Neuroscience

    (1988)
  • GraceA.A.

    Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: a hypothesis for the etiology of schizophrenia

    Neuroscience

    (1991)
  • GuoN. et al.

    Receptor mechanisms mediating clozapine-induced c-fos expression in the forebrain

    Neuroscience

    (1995)
  • HeimerL. et al.

    Specificity in the projection patterns of accumbal core and shell in the rat

    Neuroscience

    (1991)
  • KibaH. et al.

    Nicotine induced c fos expression in the striatum is mediated mostly by D1 receptor and is dependent on NMDA stimulation

    Molec. Brain Res.

    (1994)
  • LandwehrmeyerB. et al.

    Dopamine D3 receptor mRNA and binding sites in human brain

    Molec. Brain Res.

    (1993)
  • LeslieR.A. et al.

    Serotonin2/1c receptor activation causes a localized expression of the immediate-early gene c-fos in rat brain: evidence for involvement of dorsal raphe nucleus projection fibres

    Neuroscience

    (1993)
  • LindvallO.

    Mesencephalic dopaminergic afferents to the lateral septal nucleus of the rat

    Brain Res.

    (1975)
  • MacGibbonG.A. et al.

    Clozapine and haloperidol produce a differential pattern of immediate early gene expression in rat caudate-putamen, nucleus accumbens, lareral septum and islands of Calleja

    Molec. Brain Res.

    (1994)
  • MarshallJ.F. et al.

    Dopamine high-affinity transport site topography in rat brain: major differences between dorsal and ventral striatum

    Neuroscience

    (1990)
  • MengodG. et al.

    Visualization of a dopamine D1 receptor mRNA in human and rat brain

    Molec. Brain Res.

    (1991)
  • MerchantK.M.

    c-fos antisense oligonucleotide specifically attenuates haloperidol-induced increases in neurotensin/neuromedin N mRNA expression in rat dorsal striatum

    Molec. cell. Neurosci.

    (1994)
  • MorilakD.A. et al.

    Immunocytochemical localization and description of neurons expressing serotonin2 receptors in the rat brain

    Neuroscience

    (1993)
  • MuraseS. et al.

    Prefrontal cortex regulates burst firing and transmitter release in mesolimbic dopamine neurons studiedin vivo

    Neurosci. Lett.

    (1993)
  • NishinoH. et al.

    Neuronal activity in the ventral tegmental area (VTA) during motivated bar press feeding in the monkey

    Brain Res.

    (1987)
  • PennartzC.M.A. et al.

    Differential membrane properties and dopamine effects in the shell and core of the rat nucleus accumbens studiedin vitro

    Neurosci. Left.

    (1992)
  • RobertsonG.S. et al.

    D1 and D2 dopamine receptors differentially increase Fos-like immunoreactivity in accumbal projections to the ventral pallidum and midbrain

    Neuroscience

    (1995)
  • RobertsonG.S. et al.

    Neuroleptics increase c-fos expression in the forebrain: contrasting effects of haloperidol and clozapine

    Neuroscience

    (1992)
  • RobertsonG.S. et al.

    c-fos mediates antipsychotic-induced neurotensin gene expression in the rodent striatum

    Neuroscience

    (1995)
  • SegalM. et al.

    Afferents to the septal area of the rat studied with the method of retrograde axonal transport of horseradish peroxidase

    Brain Res.

    (1974)
  • StamfordJ.A. et al.

    Stimulated limbic and striatal dopamine release measured by fast cyclic voltammetry: anatomical, electrochemical and pharmacological characteristics

    Brain Res.

    (1988)
  • StamfordJ.A. et al.

    Diffusion and uptake of dopamine in rat caudate and nucleus accumbens compared using fast cyclic voltammetry

    Brain Res.

    (1988)
  • Suaud-ChagnyM.-F. et al.

    Pharmacology of electrically evoked dopamine release studied in the rat olfactory tubercle byin vivo electrochemistry

    Eur. J. Pharmac.

    (1989)
  • Suaud-ChagnyM.-F. et al.

    Relationship between dopamine release in the rat nucleus accumbens and the discharge activity of dopaminergic neurons during localin vivo application of amino acids in the ventral tegmental area

    Neuroscience

    (1992)
  • AlbaneseA. et al.

    Organization of the ascending projections from the ventral tegmental area: a multiple fluorescent retrograde tracer study in the rat

    J. comp. Neurol.

    (1983)
  • BeanA.J. et al.

    Extracellular dopamine and neurotensin in rat prefrontal cortexin vivo: effects of median forebrain bundle stimulation frequency, stimulation pattern, and dopamine autoreceptors

    J. Neurosci.

    (1991)
  • BerrettaS. et al.

    Dopamine and glutamate agonists stimulate neuron-specific expression of Fos-like protein in the striatum

    J. Neurophysiol.

    (1992)
  • BrogJ.S. et al.

    The patterns of afferent innervation of the core and shell in the “accumbens” part of the rat ventral striatum: immunohistochemical detection of retrogradely transported fluoro-gold

    J. comp. Neurol.

    (1993)
  • CalabresiP. et al.

    Synaptic and intrinsic control of membrane excitability of neostriatal neurons. I Anin vivo analysis

    J. Neurophysiol.

    (1990)
  • CharlétyP.J. et al.

    Burst firing of mesencephalic dopamine neurons is inhibited by somatodendritic application of kynurenate

    Acta physiol. scand.

    (1991)
  • CherguiK. et al.

    Subthalamic nucleus modulates burst firing of nigral dopamine neurones via NMDA receptors

    Neuroreport

    (1994)
  • CherguiK. et al.

    NMDA receptors are involved in spontaneous burst firing of dopaminergic mesencephalic neurons

    C. R. Acad. Sci. III, Paris

    (1991)
  • CherguiK. et al.

    Tonic activation of NMDA receptors causes spontaneous burst discharge of rat midbrain dopamine neuronsin vivo

    Eur. J. Neurosci.

    (1993)
  • DeutchA.Y. et al.

    The determinants of stress-induced activation of the prefrontal cortical dopamine system

  • Cited by (72)

    • Functional mechanism of ASP5736, a selective serotonin 5-HT <inf>5A</inf> receptor antagonist with potential utility for the treatment of cognitive dysfunction in schizophrenia

      2018, European Neuropsychopharmacology
      Citation Excerpt :

      DAergic neurons in the PBP, a subdivision of the VTA, largely project to the PFC while neurons in the PN, another subdivision of the VTA, project largely to the N. Acc (see Svensson et al., 1995). The major finding of our study is that in the electrophysiological experiments, ASP5736 preferentially stimulated the burst firing mode in VTA dopamine neurons, especially those located in the PBP but had no effect in the PN, indicating enhanced dopamine release and DA-D1 receptor activation in PBP target areas (see Chergui et al., 1996). In this study, 5-HT5A receptors were identified on DAergic neurons (TH-positive) and GABAergic neurons (PV-positive) in the VTA.

    • Chronic L-DOPA administration increases the firing rate but does not reverse enhanced slow frequency oscillatory activity and synchronization in substantia nigra pars reticulata neurons from 6-hydroxydopamine-lesioned rats

      2016, Neurobiology of Disease
      Citation Excerpt :

      Low frequency oscillatory activity and synchronization seem to be more important in parkinsonism because these are slightly influenced by acute and prolonged L-DOPA administration. In agreement with other studies (Murer et al., 1997; Tseng et al., 2000; Meissner et al., 2006), the present results show that the nigrostriatal lesion did not modify the firing rate of SNr neurons but changed it to become more bursting and less regular, which fits with a hyperactive neuronal discharge pattern (Chergui et al., 1996; Florin-Lechner et al., 1996). These results are on line with the increased gene expression of the cytochrome oxidase subunit, a metabolic marker of neuronal activity (Lacombe et al., 2009).

    • Lesion of the ventral tegmental area amplifies stimulation-induced Fos expression in the rat brain

      2010, Brain Research
      Citation Excerpt :

      They became susceptible for each, even weak stimulatory influences. It is known that electrical stimulation of the VTA or the medial forebrain bundle carrying its axons, induces the Fos expression mainly in the ipsilateral target structures (Arvanitogiannis et al., 1996; Chergui et al., 1996; Hunt and McGregor, 1998). However, sensitized contralateral structures could be activated even by the sparse contralateral VTA projection (Oades and Halliday, 1987) or by stimuli revealed during behavioral response to this stimulation (e.g. an odor and taste during eating response or environmental conditions during exploration).

    • Hierarchical Control of Dopamine Neuron-Firing Patterns by Nicotinic Receptors

      2006, Neuron
      Citation Excerpt :

      These networks include glutamatergic afferents, originating in part from the PFC and also the cholinergic and glutamatergic neurons in the tegmental pedunculopontine nucleus and in the laterodorsal tegmental nucleus (Kitai et al., 1999; Diana and Tepper, 2001; Floresco et al., 2003; Lodge and Grace, 2006). Even though it is now clear that multiple regulatory systems modulate DA release (Floresco et al., 2003), the burst-firing mode generates particular interest since it causes a substantially larger increase of DA release than regular spiking (Gonon, 1988) as well as a more effective activation of immediate early genes in DA target areas (Chergui et al., 1996, 1997). Furthermore, the transition from regular firing to bursting activity has been associated with alerting or anticipatory phases of reward (Schultz, 2002) or with the inappropriate stimuli of addictive drugs (Di Chiara, 2000).

    View all citing articles on Scopus
    *

    Present address: Laboratoire d'Histologie-Embryologie, CNRS EP 74, Universitéde Bordeaux II, Bordeaux, France.

    View full text