Dorsal Raphe Nucleus (DRN)

The raphe nuclei are a series of seven nuclei located in the medial portion of the reticular formation. In order from caudal to rostral, the raphe nuclei are known as the nucleus raphe obscurus, the raphe magnus, the raphe pontis, the raphe pallidus, the nucleus centralis superior, nucleus raphe dorsalis, nuclei linearis intermedius and linearis rostralis. Some scientists chose to group the linearis nuclei into one nucleus, shrinking the number of raphe to seven, e.g., NeuroNames makes the following ordering:

  Raphe nuclei of medulla
      Nucleus raphe obscurus (nucleus raphe obscurus) (B2 in Naidich)
      Nucleus raphe magnus (raphe magnus) (B3 in Naidich)
      Nucleus pallidus (raphe pallidus) (B1 in Naidich)
  Raphe nuclei of the pontine reticular formation
      Pontine raphe nucleus (raphe pontis) (B5 in Naidich)
      Inferior central nucleus (not in Naidich)
  Raphe nuclei of the midbrain reticular formation
      Superior central nucleus (nucleus centralis superior)(B6, B8 in Naidich)
      Dorsal raphe nucleus (nucleus raphe dorsalis)(B7 in Naidich)

The dorsal raphe nucleus is one of the seven bilateral brainstem nuclei located in the ventral periaqueductal grey matter of the mesencephalon, with a caudal tip projecting into the pons. The neurons of the DRN innervate a number of other regions and utilize many transmitters, of which serotonin is the most abundant and important. The DRN is involved in the control of various physiological functions and has been implicated in brain dysfunction, especially mood disorders such as depression. The human DRN has been estimated to contain approximately 235,000713,000 neurons (Baker et al., 1990). Approximately 165,000734,000 of these neurons are serotonergic (Baker et al., 1991).

Image and Location

Example image from Zambreanu et al., 2005 (Note: they don't show activation in DRN, but we clearly see the localization)

Raphe nuclei from Son et al., 2012

This figure from Son et al. 2012 clearly shows the 7 nuclei (anatomical image is from Naidich, and Son et al., 2012 combined PET and fMRI to identify clusters of glucose metabolism corresponding to those nuclei)

Naidich, T.P., Duvernoy, H.M., Delman, B.N., Sorensen, A.G., Kollias, S.S., Haacke, E.M., 2009. Duvernoy's atlas of the human brain stem and cerebellum: high-fieldMRI, surface anatomy, internal structure, vascularization and 3 D sectional anatomy. Springer, Vienna.

Son 2012

Son 2012 with text labels. Glucose metabolism, not 5HT

Neurosynth structure image:

N.A.

Neurosynth connectivity image: (Note: DRN is really close to (and probably often mislabelled in imaging studies as) PAG — it also seems to share most of its connectivity)

Searches

Searches so far:

dorsal raphe and fMRI dorsal raphe and PET dorsal raphe and connectivity dorsal raphe and optogenetics

Most important references

Structure

The raphe nuclei are at the center of serotoninergic transmission in the brain. The more dorsal nuclei project to the brain (cortex, amygdala, caudate, putamen others?). The more ventral ones project to the spine (and involved in descending modulation of pain).

The DRN seems to receive nociceptive input, but it isn't generally distinguished from the PAG.

Inputs & Outputs

(HOW DO WE ADD LINKS TO OTHER PAGES? WOULD BE NICE TO LINK THE CONNECTIONS TO THE OTHER ASSOCIATED WIKI PAGES)

(Primarily from Michelsen et al., 2008)

Efferent projections of the DRN

Serotonergic neurons of the DRN display a topographic organization along the rostrocaudal axis, with respect to efferent projections (Abrams et al., 2004). Thus, neurons located more rostrally project to more rostral areas of the brain than neurons located more caudally in the DRN. Individual neurons seem to project to several distinct but functionally related targets through branched fibres (Lowry, 2002). The first branched projections to be discovered run from the dorsal DRN along the dorsal raphe cortical tract to the substantia nigra (SN) and caudate putamen (CP) (van der Kooy and Hattori, 1980a; Imai et al., 1986). Also, single neurons have been observed to target hippocampus and entorhinal cortex (Kohler and Steinbusch, 1982), prefrontal cortex and nucleus accumbens (NA) (Van Bockstaele et al., 1993), the paraventricular nucleus (PVN) of the thalamus and the lateral parabrachial nucleus (PBN) (Petrov et al., 1992), the central nucleus of the amygdala and the PVN (Petrov et al., 1994), distinct sites in the trigeminal somatosensory pathway (Kirifides et al., 2001) and the vestibular nuclei and amygdala (Halberstadt and Balaban, 2006).

This could be a key to understanding the role of the DRN as a modulator of complex autonomic functions with anatomical correlates in several parts of the brain. For instance, both the amygdala and the PVN, which are targeted by the same branched fibres, are involved in anxiety and conditioned fear (Petrov et al., 1992, 1994). These fibres emerge from well-defined subpopulations of neurons in the medial part of the middle DRN as well as more caudal clusters. However, only a part of the neurons with branched axons contain serotonin, the reported range being between 8% (Petrov et al., 1992) and 64% (Halberstadt and Balaban, 2006) depending on the targets. This serves as a reminder that serotonin is not the only transmitter utilized by the DRN. For instance, the CeA-PVN projecting subpopulations mentioned above (where about half the neurons are serotonergic) also contain corticotropin-releasing factor (CRF), which has been associated with anxiety and other mood disorders. Anxiety-related behavioural changes induced by serotonergic activity, such as develop- ment of learned helplessness, seem to be CRF- dependent (Maier and Watkins, 2005). However, it has not been shown, whether the CRF-containing neurons themselves, or the serotonergic DRN neurons they target, send collaterals to amygdala and PVN.

Early studies showed that most DRN neurons project ipsilaterally and few contralaterally (Miller et al., 1975). Retrograde labelling studies of DRN efferents to the entorhinal cortex indicated that, when present, contralateral terminals are prefer- entially located close to the midline (Kohler and Steinbusch, 1982). Similar results were obtained recently in a study by Waselus and co-workers, in which all DRN neurons, which sent collaterals to lateral septum and striatum, were located ventromedially near the midline or slightly lateral to it. Notably, all such collateral neurons were serotonergic (Waselus et al., 2006). However, single neurons do not seem to project collaterally to both hemispheres (van der Kooy and Hattori, 1980b; Kohler and Steinbusch, 1982). Besides their topographic organization, different cell types also seem to display different projections. This has, however, not been extensively studied but is reflected in the distribution patterns of different cell types versus the projections emerging from different areas.

Pathway overview

The DRN projects along several ascending and descending pathways, most of which it shares with one or more of the other raphe nuclei. The pathway nomenclature differs slightly between authors and the division is not completely con- sistent, with some overlaps and contradictions, especially in the older literature. In this review, we have labelled the pathways according to Steinbusch et al.

Ascending pathways

There are three ascending pathways: the dorsal, medial and ventral ascending pathways (Fig. 1). Of these, the dorsal and ventral ascending pathways are the two most important efferent projections of the DRN. They reach a multitude of targets throughout the forebrain, the most important one being the CP.

Descending pathways

In addition, four descending projections leave the DRN: the bulbospinal pathway, cerebellar path- way, propriobulbar pathway and one that inner- vates the locus coeruleus, dorsal tegmental nucleus and pontine raphe nucleus. The main targets of the descending pathways are cerebellum, the lower brainstem and the spinal chord. These pathways will not be further dealt with in this chapter.

The dorsal ascending pathway

The dorsal ascending pathway rises from medial and rostral DRN. Eighty per cent of its fibres are serotonergic. It innervates the striatum and globus pallidus (GP).

Striatum

Anterograde labelling has shown that DRN effer- ents target the ventromedial striatum at caudal to midlevel (Vertes, 1991). Most striatum-projecting neurons are located in rostral DRN (Steinbusch et al., 1981). Recent retrograde labelling studies confirmed a gradient of striatum-projecting neurons in the DRN. Approximately half of the neurons were located in the rostral third of the DRN. Three out of eight neurons were seen in middle DRN, parallell to the midline, with highest concentrations dorsomedially and ventrally. Only one out of eight neurons were located in caudal DRN, in its dorsomedial part (Waselus et al., 2006). The caudate putamen (CP) is extensively innervated by neurons of the DRN. It is the single most important of targets for DRN innervation and one of the first to be extensively studied. The earliest anatomical indica- tions for DRN projections to the CP (Anden et al., 1965) were subsequently supported by lesion studies, which showed a drop in striatal TPH activity (Geyer et al., 1976) as well as a decrease in [3H]5-HT uptake (Kellar et al., 1977) after DRN leisons, and by in vivo microdialysis, which showed that electrical stimulation of the DRN lead to a rise in serotonin dialysate in the CP (McQuade and Sharp, 1997). Meanwhile, more anatomical data has accumulated. Approximately one-third of all serotonergic DRN neurons project to the CP. This is, however, region-specific: in a cluster in dorsomedial DRN, 80–90% of seroto- nergic neurons were found to project to the CP (Steinbusch et al., 1981). In addition, 80% of DRN neurons that project to the CP are seroto- nergic, and they mainly project ipsilaterally. The remaining 20% of non-serotonergic CP-projecting neurons are mostly found in the caudal parts of ventromedian and dorsomedian DRN (see Fig. 2 for an overview of DRN anatomy).

The innervation of NA is even higher than that of the CP. A majority of the innervation is serotoner- gic. The shell of the NA is more heavily innervated than the core, especially in more caudal regions where the fibres in the shell are much more abundant than elsewhere in the NA. The core is innervated exclusively by thin (0.3 mm) smooth axons, similar to the rostral shell, which is innervated predominantly by thin axons and, to a lesser extent, by varicose fibres. In contrast, the caudal shell is innervated predominantly by thicker, highly varicose (0.5 mm between varicosities) sero- tonergic axons (Van Bockstaele and Pickel, 1993; Brown and Molliver, 2000). It has not been determined that all the innervation indeed stems from the DRN. However, studies on projections to cerebral cortex and olfactory bulb have shown that thin drug-sensitive serotonin axons typically arise from the DRN and varicose, drug-resistant axons arise from the MRN (Kosofsky and Molliver, 1987; Mamounas et al., 1991). In NA, the thin fibres of the core are more vulnerable to amphetamine derivatives than the thick fibres of the shell, indicating that the DRN innervates the NA core, as suggested by Brown and Molliver (2000).

Globus pallidus

Pallidal afferents from DRN have been demon- strated by tracing studies. Vertes (1991) used the retrograde tracer PHA-L in rats and DeVito et al. (1980) used the anterograde tracer HRP in macaque monkeys. The innervation of GP is mainly serotonergic, as confirmed by micro- dialysis studies in the rat, where stimulation of the DRN increased serotonin dialysate in the GP by 75%. In the same study, stimulation of the MRN had little or no effect (McQuade and Sharp, 1997).

Medial ascending pathway

The main target of the medial ascending pathway is SN. To a lesser extent, the pathway also innervates the CP. The fibres emerge from rostral parts of the DRN (van der Kooy and Hattori, 1980a; Imai et al., 1986).

Substantia nigra

Studies with the retrograde tracer HRP injected to the SN showed labelled neurons in the DRN but not in the MRN (Bunney and Aghajanian, 1976; Fibiger and Miller, 1977). The projections seem to arise from rostral DRN (Imai et al., 1986) and they target the pars compacta division in particular, whereas the pars reticulata seems to be innervated to a lesser, yet substantial degree, as indicated by studies using [3H]leucine (Fibiger and Miller, 1977) and [14C]leucine (Bobillier et al., 1976) injections into the DRN. However, a study using the retrograde tracer PHA-L failed to demonstrate DRN innervation of the pars reticulata (Vertes, 1991).

Caudate-putamen

Although the dorsal ascending pathway conveys most of the raphe input to the CP, it also receives innervation via the medial ascending pathway. Some of the fibres branch and target both the SN and CP (van der Kooy and Hattori, 1980a; Imai et al., 1986). Thus, single DRN neurons can exert control over both the SN and the CP.

Ventral ascending pathway

Via the ventral ascending pathway, the DRN innervates many areas. The bilateral pathway ascends ventrolaterally and then turns rostrally to enter the medial forebrain bundle. The pathway also contains fibres from other raphe nuclei, especially the MRN. The main targets are thalamic and hypothalamic nuclei, habenula, septum, amygdala, cortex, the olfactory bulb, hippocam- pus, interpeduncular nucleus and geniculate body.  Hypothalamus

Several studies have addressed the projections from the raphe nuclei to the hypothalamus. In an early autoradiographic study, in which [14C] tracing was used to map DRN efferents in cat, Bobillier et al. (1976) identified varying degrees of DRN innervation in several hypotha- lamic nuclei. Most of these results were later confirmed, while some have been contradicted by subsequent experiments. In addition, some studies have not distinguished between the raphe subnuclei. For instance Steinbusch and Nieuwenhuys (1982) demonstrated serotonergic innervation in nearly all parts of the hypothala- mus, but they did not attempt to locate the projecting perikarya. Some studies have indicated that the MRN is a greater source of hypothalamic serotonin innervation than the DRN (Geyer et al., 1976; Kellar et al., 1977).

The DRN has been reported to innervate the SCN and preoptic area (Bobillier et al., 1976), but later studies in the rat suggest that DRN does not project to these structures (van de Kar and Lorens, 1979; Meyer-Bernstein and Morin, 1996). The dense serotonergic innervation of the SCN and medial preoptic area (Bobillier et al., 1976), and the light-to-moderate serotonergic innervation of the rest of the anterior hypotha- lamus, seems to emerge from the MRN instead (van de Kar and Lorens, 1979; Hay-Schmidt et al., 2003).

Tracings studies have identified moderate DRN innervation in posterior hypothalamus (Bobillier et al., 1976) and lesion studies have shown that the arcuate nucleus receives innervation from DRN (van de Kar and Lorens, 1979). Further- more, the lateral hypothalamus receives high innervation from the DRN. This was shown by early [14C] tracing studies, such as by Bobillier et al. (1976) and later confirmed with PHA-L tracing (Vertes, 1991). A recent anterograde tracing study showed that neurons in the central portion of the rostral DR innervate about 23% of the orexinergic neurons of the lateral hypothala- mus, mainly in the lateral parts of the cluster (Yoshida et al., 2006).

Thalamus

Several of the thalamic nuclei receive innervation from the DRN. Studies in cat and rat have reported dense innervation in the midline and intralaminar nuclei of the thalamus (including the posterior paraventricular, the parafascicular, reuniens, rhomboid, intermediodorsal/mediodor- sal and central medial thalamic nuclei) and moderate innervation in thalamic paracentral and central lateral intralaminar nuclei (Conrad et al., 1974; Bobillier et al., 1976; Vertes, 1991). In addition, the subparafascicular and prethalamic nuclei (Bobillier et al., 1976) have been reported to receive innervation from the DRN, but confirma- tion by later studies is lacking.

Habenula

The DRN innervates the lateral habenula to a moderate extent, whereas the medial habenula does not seem to receive any innervation in rat (Sim and Joseph, 1993), cat (Bobillier et al., 1976) and hamster (Morin and Meyer-Bernstein, 1999). One study, however, reported low innervation in the medial habenula of rat (Morin and Meyer- Bernstein, 1999). In the same study the hamster lateral habenula was shown to receive only sparse serotonergic innervation, indicating that the input from DRN is mainly non-serotonergic.

Septum

The DRN sends strong innervation to the lateral septum, 80% of which is serotonergic (Kohler et al., 1982). The innervation predominantly targets the medial portions of the lateral septum (Vertes, 1991). Most of the projecting neurons are located throughout the caudal DRN. In the rest of the DRN, neurons are sparse and located ventromedially. The neuron number decreases towards the mid-DRN and is very low in rostral DRN, while most of the rostral parts contain no septum-projecting neurons at all (Waselus et al., 2006). The medial septum is not generally considered a target of DRN innervation. Micro- dialysis studies have, however, shown that stimu- lation of DRN can increase serotonin dialysate in medial septum by more than 55%. This suggests that the DRN does indeed target the area, but as long as anatomical evidence is lacking it can not be excluded that such measurements actually sample serotonin from the lateral septum (McQuade and Sharp, 1997).

Amygdaloid complex

Studies using neuronal tracers, PHA-L in parti- cular, have demonstrated that the basolateral and lateral amygdaloid nuclei, as well as the extended amygdala (comprising centromedial amygdala + bed nucleus of stria terminalis and substantia innomi- nata, as defined by Alheid and Heimer, 1988) receive dense innervation from the DRN (Grove, 1988; Vertes, 1991). Also, immunohistochemical techniques in rat have shown that the basolateral amygdaloid nuclei receive strong serotonergic innervation, especially the rostral and medial parts of the basal nucleus, while the caudal part of the basal nucleus as well as the entire lateral nucleus receive a lower, yet high density of serotonin innervation. In the centromedial nuclei innervation is very low, except for the posterior part of the medial amygdaloid nucleus and the medial and lateral parts of the posterior nucleus (Steinbusch, 1981). The serotonin-immunoreactivity in the amygdaloid has not been directly correlated to DRN efferents. However, in squirrel monkeys, the most abundant serotonergic fibre type is thin, with fusiform or pleiomorphic varicosities, which suggests that serotonergic innervation emerges predomi- nantly from the DRN (Sadikot and Parent, 1990). A more recent immunohistochemical study in macaque monkeys is not consistent with the rat data, with regard to the relative fibre density in amygdaloid subnuclei, probably due to species diffe- rences. The highest levels were present in lateral subregions of the central amygdala and dorsolateral bed nucleus of stria terminalis. Levels were high in basal amygdala and moderate in centromedial amygdaloid nuclei (Freedman and Shi, 2001).

Cerebral Cortex

Several studies have dealt with cortical projections of the DRN (Bobillier et al., 1976; O’Hearn and Molliver, 1984; Vertes, 1991). O’Hearn and Molliver demonstrated that the cortical projections of rat DRN emerge predominantly from the ventral subnucleus, in particular from immediately dorsal or medial to the medial longitudinal fasciculi. These areas account for three-fourths of the DRN inner- vation of the cortex, whereas the dorsal subnucleus contributes one-fourth. Along the rostrocaudal axis, most neurons are located in the middle DRN, and the lateral areas of the DRN do not seem to project to the cerebral cortex at all. More than 80% of the projections are serotonergic (O’Hearn and Molliver, 1984). The ratio of contralateral fibres is 26–35%, and differs between the subnuclei. At least in entorhinal cortex, the contralateral fibres seem to preferentially target medial areas (Kohler and Steinbusch, 1982; O’Hearn and Molliver, 1984).

The frontal cortex receives most of its serotonergic innervation from the DRN (Kosofsky and Molliver, 1987). The density is highest in the dorsal frontal cortex and low in caudal regions, with intermediate densities in areas in between (Steinbusch, 1981). The frontal cortex receives projections from nearly twice as many DRN neurons as either the parietal or occipital cortex (O’Hearn and Molliver, 1984). The entorhinal cortex is targeted by both serotonergic and non-serotonergic projections (Segal, 1977) and (Koh- ler and Steinbusch, 1982) which for the most part emerge from the DRN (Kohler and Steinbusch, 1982). In addition, anterograde labellings with PHA- L have shown that many cortical regions receive dense (the piriform, insular and frontal cortices) or moderately dense (occipital, entorhinal, perirhinal, frontal orbital, anterior cingulate and infralimbic cortices) projections from the DRN (Vertes, 1991).

Hippocampus

DRN projects to the hippocampus (Segal and Landis, 1974; Azmitia and Segal, 1978). DRN efferents to the hippocampus emerge predominantly from the most caudal parts of the nucleus, close to the midline, and is both serotonergic and non- serotonergic (Wyss et al., 1979; Kohler and Stein- busch, 1982). Immunohistochemical stainings have demonstrated fine serotonergic axons with small varicosities throughout the hippocampus (Fig. 3). The fibres’ morphology (Kosofsky and Molliver, 1987) suggests that they derive from the DRN (Mamounas et al., 1991). However, lesion studies have indicated that the MRN and not the DRN is the major source of hippocampal serotonin innerva- tion (van de Kar and Lorens, 1979).

Olfactory bulb

Tracing studies with radioactively labelled amino acids in rat (Halaris et al., 1976) and cat (Bobillier et al., 1976) have demonstrated DRN projections to the olfactory bulb. The DRN is the primary source of serotonin in the olfactory bulb, as shown by retrograde transport of [3H]serotonin (Araneda et al., 1980a, b). Immunohistochemical stainings have demonstrated serotonergic innervation of all layers of the olfactory bulb, especially the glome- rular lamina (Steinbusch, 1981).

Supraependymal plexus

The supraependymal plexus is a network of serotonergic fibres, which covers nearly all ventri- cular surfaces with moderate or high density. They are most numerous in the third ventricle and the foramina of Monro, fewer in the lateral ventricles and aqueduct and numerous in the hypothalamic region of the third ventricle. Areas with low density or absence of fibres are the third ventricle floor, the preoptic area, the roof of interventricular foramen, the subfornical organ and the roof of the fourth ventricle (Richards et al., 1973; Chan-Palay, 1976; Lorez and Richards, 1982). The plexus was discovered already in the 1920s (Lorez and Richards, 1982) and later identified as being mainly serotonergic (Richards et al., 1973).

Several studies have indicated that the suprae-pendymal serotonergic fibres ascend from the medial and in particular, dorsal raphe: in rats, supraependymal fibres degenerated after lesions of the dorsal and medial raphe (Aghajanian and Gallager, 1975), and electrical stimulation of the medial and pontine raphe led to an increase in [3H]5-HT uptake from the intracerebroventricular space (Chan-Palay, 1976). Also [125I] tetanus toxin was injected into the lateral ventricles labelled neurons of the medial and dorsal raphe by means of retrograde transport along the fibres (Richards, 1978). Further, there is a direct fibre pathway between the DRN and the aqueduct surface in rats (Steinbusch et al., 1981), and in mice, an exit zone for fibres to the fourth ventricle has been reported immediately dorsal to the DRN (Derer, 1981). In cats, a [3H]-labelled proline injection in DRN and raphe centralis superior labelled supraependymal surfaces of all ventricles by means of anterograde transport (Pierce et al., 1976).

Studies on the rat lateral ventricles indicate that serotonergic fibres do not penetrate the ependyma, but instead enter the ventricles from their rostral poles. These fibres travel along fibres that travel through the median forebrain bundle and turn dorsocaudally between the CP and corpus callo- sum. Also, they do not form synaptic contact with ependymal cells. They are not found between ependyma and subependyma, but only in the lateral ventricles (Dinopoulos et al., 1995).

Neurotransmitters

DRN neurons utilize several other neurotransmit- ters (Fig. 3). This chapter will list such transmit- ters, but not those, which are located in afferent fibres to the DRN and synthesized elsewhere.

Serotonin

Serotonin is the main neurotransmitter of the DRN and the first one to be demonstrated there (Dahlstrom and Fuxe, 1964). The serotonergic DRN neurons and their projections have been described in more detail in other parts of this chapter.

Dopamine

Dopamine was one of the first transmitters, to be demonstrated in DRN neurons, first with histo- fluorescence methods (Lindvall and Bjorklund, 1974; Ochi and shimizu, 1978) and later with antibodies against tyrosine hydroxylase (TH) and dopamine-b-hydroxylase (DbH) (Nagatsu et al., 1979). These dopaminergic neurons are located preferentially in ventromedial parts. They mainly target the NA and lateral septum, and to a lesser extent medial prefrontal cortex. In addition, very few fibres project to CP (Stratford and Wirtshafter, 1990).

GABA

GABAergic neurons were first demonstrated in the DRN by radioautographic tracing and GABA-uptake (Belin et al., 1979). The observa- tion was supported by immunohistochemistry with an antibody against the GABA-synthesizing enzyme g-aminobutyric acid decarboxylase, or GAD (Mugnaini and Oertel, 1985) and the GABA-degrading enzyme GABA-transaminase, or GABA-T (Nagai et al., 1983). The GABAergic synapse with serotonergic DRN neurons (Wang et al., 1992). They are markedly smaller than most serotonergic neurons and fire spikes characterized by short width and high frequency (Allers and Sharp, 2003).

Peptide transmitters

Immunohistochemical stainings have shown that the DRN harbours neuropeptide Y (NPY) con- taining neurons, most of which are medium-sized, fusiform and bipolar (de Quidt and Emson, 1986). In situ-hybridization has demonstrated the pre- sence of NPY mRNA in the DRN (Pau et al., 1998).

Substance P has been shown to colocalize with serotonin in the DRN in at least rat (Chan-Palay et al., 1978; Hokfelt et al., 1978), cat (Lovick and Hunt, 1983; Arvidsson et al., 1994) and human (Baker et al., 1990, 1991). Substance P also colocalizes with serotonin in ascending projec- tions, but such fibres have not been shown to arise from the DRN (Otake, 2005). However, in another study no colocalization was seen in ascending fibres (Rupniak and Kramer, 1999). Low levels of prepro-galanin mRNA are present in DRN neurons (Cortes et al., 1990), yet galanin itself has been detected with immunohistochemistry only after colchicine treatment (Skofitsch and Jacobowitz, 1985). Galanin colocalizes with seroto- nin in the DRN. In fact, it has been reported that a large proportion of serotonergic DRN neurons also contain galanin (Melander et al., 1986). Galanin is also present in serotonergic fibres in one of the target areas of the DRN, the cortex (Skofitsch and Jacobowitz, 1985), but it has not been confirmed that these projections arise in the DRN.

Enkephalin (ENK)-containing neurons were first reported in the dorsal and lateral parts of rat DRN, just adjacent to the periventricular grey matter (Hokfelt et al., 1977; Uhl et al., 1979). Immunohistochemical studies showed that ENK is present throughout the cat DRN in neurons of variable morphology (Moss et al., 1980, 1981). However, serotonergic double-labelled neurons were predominantly small and round and located at the midline, dorsal to the medial longitudinal fasciculus (Glazer et al., 1981).

CRF immunoreactivity has been demonstrated in DRN neurons after colchicine treatment (Commons et al., 2003). CRF-immunoreactive neurons were mainly clustered in the dorsomedial subregion, especially in the middle DRN. Scattered neurons were seen in the lateral wings, while they were largely absent from the ventromedial DRN and the most caudal part of the DRN. Most (B96%) of CRF-immunoreactive neurons in the dorsomedial DRN were serotonergic, as defined by immuno- reactivity for TPH. Anterograde tracing (PHA-L) indicated that neurons in the middle portion of the dorsomedial DRN mainly target the CeA, the dorsal hypothalamic area and the bed nucleus of the stria terminalis (Commons et al., 2003).

In additional vasoactive intestinal polypeptide (VIP) has been demonstrated in neurons of both rat and mouse DRN (Sims et al., 1980) and cholecystokinin (CKK)-containing neurons in the rat DRN have been shown to innervate the PVN of the thalamus (Bhatnagar et al., 2000; Otake, 2005).

Glutamate

Phosphate-activated glutaminase (PAG) has been de- monstrated in TH-, DbH- or phenylethanolamine-N- methyltransferase (PNMT)-immunoreactive neurons, suggesting that glutamate is formed from glutamine in serotonergic and catecholaminergic neurons of the DRN (Kaneko et al., 1990).

Nitric oxide

The presence of nitric oxide (NO) in DRN was first demonstrated by immunohistochemistry against the NO synthesis reaction product citrul- line (Pasqualotto et al., 1991) and against argini- nosuccinate synthetase which turns citrulline into argininosuccinate (Nakamura et al., 1991). Subse- quently, the presence of NO in both serotonergic and non-serotonergic DRN neurons was demon- strated by colocalization of serotonin-immuno- reactivity with immunoreactivity for NO synthase (NOS) (Dun et al., 1994; Rodrigo et al., 1994) or with NADPH diaphorase activity (Johnson and Ma, 1993; Wotherspoon et al., 1994). The NO- synthesizing neurons are predominantly clustered in medioventral and mediodorsal parts of DRN (Wang et al., 1995). In the medial subnuclei, between 23 and 38% of serotonergic neurons appear to synthesize NO, whereas 60–77% of NO-synthesizing neurons are serotonergic. In the lateral subregions, NADPH diaphorase activity is present, but its activity does not overlap with serotonergic neurons (Wotherspoon et al., 1994).

Transient presence of additional transmitters

At least two additional neurotransmitters have been reported in the developing, but not adult, DRN. Histamine is present in neurons of rat and mouse DRN during embryonic development, but disappears before birth, as demonstrated by the presence of histamine-immunoreactivity and histi- dine decarboxylase (the histamine-synthesizing enzyme) mRNA (Auvinen and Panula, 1988; Nissinen and Panula, 1995; Nissinen et al., 1995; Karlstedt et al., 2001). Recent studies have shown that the gastrointestinal peptide secretin is also present in the DRN during mouse embryonic development (Lossi et al., 2004).

Effects of stimulation

In vivo microdialysis showed that electrical stimulation of the DRN lead to a rise in serotonin dialysate in the caudate putamen. The innervation of globes pallidus is mainly serotonergic, as confirmed by microdialysis studies in the rat, where stimulation of the DRN increased serotonin dialysate in the GP by 75%. In the same study, stimulation of the MRN had little or no effect. The medial septum is not generally considered a target of DRN innervation. Micro- dialysis studies have, however, shown that stimulation of DRN can increase serotonin dialysate in medial septum by more than 55%. This suggests that the DRN does indeed target the area, but as long as anatomical evidence is lacking it can not be excluded that such measurements actually sample serotonin from the lateral septum McQuade, R. and Sharp, T. (1997) Functional mapping of dorsal and median raphe 5-hydroxytryptamine pathways in forebrain of the rat using microdialysis. J. Neurochem., 69: 791–796.

Electrical stimulation of the medial and pontine raphe led to an increase in [3H]5-HT uptake from the intracerebroventricular space. Chan-Palay, V. (1976) Serotonin axons in the supra- and subependymal plexuses and in the leptomeninges; their roles in local alterations of cerebrospinal fluid and vasomotor activity. Brain Res., 102: 103–130.

Acute 8-OH-DPAT administration, under conditions known to suppress raphe neuronal firing, also reduced VCMs. Immediate early gene mapping using zif268 in situ hybridization revealed that STN-DBS inhibited activity of DRN and MRN neurons. Creed MC, Hamani C, Bridgman A, Fletcher PJ, Nobrega JN. Contribution of decreased serotonin release to the antidyskinetic effects of deep brain stimulation in a rodent model of tardive dyskinesia: comparison of the subthalamic and entopeduncular nuclei. J Neurosci. 2012 Jul 11;32(28):9574-81.

Vagus nerve stimulation (VNS) is an adjunctive treatment for resistant epilepsy and depression. Electrophysiological recordings in the rat brain have already shown that chronic VNS increases norepinephrine (NE) neuronal firing activity and, subsequently, that of serotonin (5-HT) neurons through an activation of their excitatory α1-adrenoceptors. Chronic VNS significantly increased extracellular 5-HT levels in the dorsal raphe but not in the hippocampus and prefrontal cortex. In conclusion, the effect of VNS in increasing the transmission of monoaminergic systems targeted in the treatment of resistant depression should be involved, at least in part, in its antidepressant properties observed in patients not responding to many antidepressant strategies. Manta S, El Mansari M, Debonnel G, Blier P..“Electrophysiological and neurochemical effects of long-term vagus nerve stimulation on the rat monoaminergic systems.” Int J Neuropsychopharmacol. 2012 Apr 17:1-12. [Epub ahead of print]

Previous studies have suggested that serotonergic neurons in the midbrain raphe complex have a functional topographic organization. Recent studies suggest that stimulation of a bed nucleus of the stria terminalis-dorsal raphe nucleus pathway by stress- and anxiety-related stimuli modulates a subpopulation of serotonergic neurons in the dorsal part of the dorsal raphe nucleus (DRD) and caudal part of the dorsal raphe nucleus (DRC) that participates in facilitation of anxiety-like responses. In contrast, recent studies suggest that activation of a spinoparabrachial pathway by peripheral thermal or immune stimuli excites subpopulations of serotonergic neurons in the ventrolateral part of the dorsal raphe nucleus/ventrolateral periaqueducal gray (DRVL/VLPAG) region and interfascicular part of the dorsal raphe nucleus (DRI). Studies support a role for serotonergic neurons in the DRVL/VLPAG in inhibition of panic-like responses, and serotonergic neurons in the DRI in antidepressant-like effects. Thus, data suggest that while some subpopulations of serotonergic neurons in the dorsal raphe nucleus play a role in facilitation of anxiety-like responses, others play a role in inhibition of anxiety- or panic-like responses, while others play a role in antidepressant-like effects. Understanding the anatomical and functional properties of these distinct serotonergic systems may lead to novel therapeutic strategies for the prevention and/or treatment of affective and anxiety disorders. In this review, we describe the anatomical and functional properties of subpopulations of serotonergic neurons in the dorsal raphe nucleus, with a focus on those implicated in symptoms of anxiety and affective disorders, the DRD/DRC, DRVL/VLPAG, and DRI. Hale MW, Shekhar A, Lowry CA. Stress-related Serotonergic Systems: Implications for Symptomatology of Anxiety and Affective Disorders.Cell Mol Neurobiol. 2012 Jul;32(5):695-708. Epub 2012 Apr 7.

Tonic immobility (TI) is an innate defensive behavior that can be elicited by physical restriction and postural inversion and is characterized by a profound and temporary state of akinesis. Our previous studies demonstrated that the stimulation of serotonin receptors in the dorsal raphe nucleus (DRN) appears to be biphasic during TI responses in guinea pigs (Cavia porcellus). Serotonin released by the DRN modulates behavioral responses and its release can occur through the action of different neurotransmitter systems, including the opioidergic and GABAergic systems. This study examines the role of opioidergic, GABAergic and serotonergic signaling in the DRN in TI defensive behavioral responses in guinea pigs. Microinjection of morphine (1.1 nmol) or bicuculline (0.5 nmol) into the DRN increased the duration of TI. The effect of morphine (1.1 nmol) was antagonized by pretreatment with naloxone (0.7 nmol), suggesting that the activation of μ opioid receptors in the DRN facilitates the TI response. By contrast, microinjection of muscimol (0.5 nmol) into the DRN decreased the duration of TI. However, a dose of muscimol (0.26 nmol) that alone did not affect TI, was sufficient to inhibit the effect of morphine (1.1 nmol) on TI, indicating that GABAergic and enkephalinergic neurons interact in the DRN. Microinjection of alpha-methyl-5-HT (1.6 nmol), a 5-HT(2) agonist, into the DRN also increased TI. This effect was inhibited by the prior administration of naloxone (0.7 nmol). Microinjection of 8-OH-DPAT (1.3 nmol) also blocked the increase of TI promoted by morphine (1.1 nmol). Our results indicate that the opioidergic, GABAergic and serotonergic systems in the DRN are important for modulation of defensive behavioral responses of TI. Therefore, we suggest that opioid inhibition of GABAergic neurons results in disinhibition of serotonergic neurons and this is the mechanism by which opioids could enhance TI. Conversely, a decrease in TI could occur through the activation of GABAergic interneurons. Ferreira MD, Menescal-de-Oliveira L. Opioidergic, GABAergic and serotonergic neurotransmission in the dorsal raphe nucleus modulates tonic immobility in guinea pigs.Physiol Behav. 2012 May 15;106(2):109-16. Epub 2012 Jan 12.

Effects of lesions/inactivation

  • List with references.
  • Unordered List Item

Effects of microinjection

  • List with references.
  • Unordered List Item

Optogenetics

Understanding serotonergic (5-HT) signaling is critical for understanding human physiology, behavior, and neuropsychiatric disease. 5-HT mediates its actions via ionotropic and metabotropic 5-HT receptors. The 5-HT(1A) receptor is a metabotropic G protein-coupled receptor linked to the G(i/o) signaling pathway and has been specifically implicated in the pathogenesis of depression and anxiety. To understand and precisely control 5-HT(1A) signaling, we created a light-activated G protein-coupled receptor that targets into 5-HT(1A) receptor domains and substitutes for endogenous 5-HT(1A) receptors. To induce 5-HT(1A)-like targeting, vertebrate rhodopsin was tagged with the C-terminal domain (CT) of 5-HT(1A) (Rh-CT(5-HT1A)). Rh-CT(5-HT1A) activates G protein-coupled inward rectifying K(+) channels in response to light and causes membrane hyperpolarization in hippocampal neurons, similar to the agonist-induced responses of the 5-HT(1A) receptor. The intracellular distribution of Rh-CT(5-HT1A) resembles that of the 5-HT(1A) receptor; Rh-CT(5-HT1A) localizes to somatodendritic sites and is efficiently trafficked to distal dendritic processes. Additionally, neuronal expression of Rh-CT(5-HT1A), but not Rh, decreases 5-HT(1A) agonist sensitivity, suggesting that Rh-CT(5-HT1A) and 5-HT(1A) receptors compete to interact with the same trafficking machinery. Finally, Rh-CT(5-HT1A) is able to rescue 5-HT(1A) signaling of 5-HT(1A) KO mice in cultured neurons and in slices of the dorsal raphe showing that Rh-CT(5-HT1A) is able to functionally compensate for native 5-HT(1A). Thus, as an optogenetic tool, Rh-CT(5-HT1A) has the potential to directly correlate in vivo 5-HT(1A) signaling with 5-HT neuron activity and behavior in both normal animals and animal models of neuropsychiatric disease. Oh, E., Maejima, T., Liu, C., Deneris, E.S., and Herlitze, S. (2010). Substitution of 5-HT1A receptor signaling by a light-activated G protein-coupled receptor. J. Biol. Chem. 285, 30825–30836.

Orexin/hypocretin neurons have a crucial role in the regulation of sleep and wakefulness. To help determine how these neurons promote wakefulness, we generated transgenic mice in which orexin neurons expressed halorhodopsin (orexin/Halo mice), an orange light-activated neuronal silencer. Slice patch-clamp recordings of orexin neurons that expressed halorhodopsin demonstrated that orange light photic illumination immediately hyperpolarized membrane potential and inhibited orexin neuron discharge in proportion to illumination intensity. Acute silencing of orexin neurons in vivo during the day (the inactive period) induced synchronization of the electroencephalogram and a reduction in amplitude of the electromyogram that is characteristic of slow-wave sleep (SWS). In contrast, orexin neuron photoinhibition was ineffective during the night (active period). Acute photoinhibition of orexin neurons during the day in orexin/Halo mice also reduced discharge of neurons in an orexin terminal field, the dorsal raphe (DR) nucleus. However, serotonergic DR neurons exhibited normal discharge rates in mice lacking orexin neurons. Thus, although usually highly dependent on orexin neuronal activity, serotonergic DR neuronal activity can be regulated appropriately in the chronic absence of orexin input. Together, these results demonstrate that acute inhibition of orexin neurons results in time-of-day-dependent induction of SWS and in reduced firing rate of neurons in an efferent projection site thought to be involved in arousal state regulation. The results presented here advance our understanding of the role of orexin neurons in the regulation of sleep/wakefulness and may be relevant to the mechanisms that underlie symptom progression in narcolepsy. Tsunematsu, T. et al. (2011) Acute optogenetic silencing of orexin/ hypocretin neurons induces slow-wave sleep in mice. J. Neurosci. 31, 10529–10539

Other

Studies activating

Coordinates

Coordinates (x, y, z): [0, 0, 0] , [0, 0, 0] Say how overall coordinates were derived here (single study? average? structural landmark?)

Specific study coordinates (if not too many)

Study Description x y z
Napadow 2005 Contrast Descrip 0 -21 -4
Pedroni 2011 Contrast Descrip -2 -32 -16
Kalin 2005 Contrast Descrip -1 -14 -4

List of Studies

Specific, key studies

Michelson et al., 2008. The dorsal raphe nucleus and serotonin: implications for neuroplasticity linked to major depression and Alzheimer’s disease. michelsen_2008.pdf

Napadow et al., 2005 Correlating Acupuncture fMRI in the Human Brainstem with Heart Rate Variability. 27th Annual International IEEE EMBS Conference; Shanghai, China.

napadow_2005.pdf

Pedroni et al., 2011: DRN activity correlates (PPI) with decreases in nACC when rewards are omitted (negative PE). Nice discussion on how this might relate to RCZ showing the same pattern (DRN serotonin decreases striatal dopamine which releases inhibition on RCZ), in relation with error-related negativity in ERP studies. lOFC (which could be considered as ant insula) also show the same pattern as the DRN.

pedroni2011.pdf

Kalin et al., 2005: DRN activity correlates with contextual (adaptive) freezing in monkeys

kalin2005.pdf

Tanaka et al., 2004: DRN associated with a condition in which large delayed rewards are associated with small immediate losses. Their interpretation is mainly oriented towards the idea that DRN is encoding the delayed reward (and inhibition of immediate response), but it could be that DRN activity is explained by the frequent losses

tanaka_et_al_2004.pdf

Study list: Coordinate based

Neurosynth results for coordinate(s)

Studies reporting activation within 10 mm of (0, -20, -4):

'Do I like this person?' A network analysis of midline cortex during a social preference task Chen AC; Welsh RC; Liberzon I; Taylor SF NeuroImage 2010 20188190

A cerebellar thalamic cortical circuit for error-related cognitive control Ide JS; Li CS NeuroImage 2011 20656038

A comparison of brain activation patterns during covert and overt paced auditory serial addition test tasks Forn C; Ventura-Campos N; Belenguer A; Belloch V; Parcet MA; Avila C Human Brain Mapping 2008 17598164

A cross-modal system linking primary auditory and visual cortices: Evidence from intrinsic fMRI connectivity analysis Eckert MA; Kamdar NV; Chang CE; Beckmann CF; Greicius MD; Menon V Human Brain Mapping 2008 18412133

A functional dissociation of conflict processing within anterior cingulate cortex Kim C; Kroger JK; Kim J Human Brain Mapping 2010 21229616

A functional magnetic resonance imaging study of working memory abnormalities in schizophrenia Johnson MR; Morris NA; Astur RS; Calhoun VD; Mathalon DH; Kiehl KA; Pearlson GD Biological Psychiatry 2006 16503328

A regulation role of the prefrontal cortex in the fist-edge-palm task: evidence from functional connectivity analysis Rao H; Di X; Chan RC; Ding Y; Ye B; Gao D NeuroImage 2008 18495496

A supramodal limbic-paralimbic-neocortical network supports goal-directed stimulus processing Laurens KR; Kiehl KA; Liddle PF Human Brain Mapping 2005 15593271

Abnormal activity patterns in premotor cortex during sequence learning in autistic patients Muller RA; Cauich C; Rubio MA; Mizuno A; Courchesne E Biological Psychiatry 2004 15336514

Abnormal object recall and anterior cingulate overactivation correlate with formal thought disorder in schizophrenia Assaf M; Rivkin PR; Kuzu CH; Calhoun VD; Kraut MA; Groth KM; Yassa MA; Hart J Jr; Pearlson GD Biological Psychiatry 2006 16199012

Abnormal temporal difference reward-learning signals in major depression Kumar P; Waiter G; Ahearn T; Milders M; Reid I; Steele JD Brain 2008 18579575

Absolute coding of stimulus novelty in the human substantia nigra/VTA Bunzeck N; Duzel E Neuron 2006 16880131

Action selection: a race model for selected and non-selected actions distinguishes the contribution of premotor and prefrontal areas Rowe JB; Hughes L; Nimmo-Smith I NeuroImage 2010 20188184

Activation in striatum and medial temporal lobe during sequence learning in younger and older adults: relations to performance Rieckmann A; Fischer H; Backman L NeuroImage 2010 20079855

Acupuncture modulates spontaneous activities in the anticorrelated resting brain networks Bai L; Qin W; Tian J; Dong M; Pan X; Chen P; Dai J; Yang W; Liu Y Brain Research 2009 19427842

Adult age differences in functional connectivity during executive control Madden DJ; Costello MC; Dennis NA; Davis SW; Shepler AM; Spaniol J; Bucur B; Cabeza R NeuroImage 2010 20434565

Age-dependent changes in the neural correlates of force modulation: an fMRI study Ward NS; Swayne OB; Newton JM Neurobiology of Aging 2008 17566608

Age-related differences in brain activity during verbal recency memory Rajah MN; McIntosh AR Brain Research 2008 18282558

Age-related functional changes in gustatory and reward processing regions: An fMRI study Jacobson A; Green E; Murphy C NeuroImage 2010 20472070

Age-related functional recruitment for famous name recognition: an event-related fMRI study Nielson KA; Douville KL; Seidenberg M; Woodard JL; Miller SK; Franczak M; Antuono P; Rao SM Neurobiology of Aging 2006 16225965

Aging and the interaction of sensory cortical function and structure Peiffer AM; Hugenschmidt CE; Maldjian JA; Casanova R; Srikanth R; Hayasaka S; Burdette JH; Kraft RA; Laurienti PJ Human Brain Mapping 2009 18072271

Altered brain activity during pain processing in fibromyalgia Burgmer M; Pogatzki-Zahn E; Gaubitz M; Wessoleck E; Heuft G; Pfleiderer B NeuroImage 2009 18848998

Amygdala activation and facial expressions: explicit emotion discrimination versus implicit emotion processing Habel U; Windischberger C; Derntl B; Robinson S; Kryspin-Exner I; Gur RC; Moser E Neuropsychologia 2007 17408704

Amygdala and nucleus accumbens in responses to receipt and omission of gains in adults and adolescents Ernst M; Nelson EE; Jazbec S; McClure EB; Monk CS; Leibenluft E; Blair J; Pine DS NeuroImage 2005 15850746

Amygdala and orbitofrontal reactivity to social threat in individuals with impulsive aggression Coccaro EF; McCloskey MS; Fitzgerald DA; Phan KL Biological Psychiatry 2007 17210136

An event-related fMRI study of the neural networks underlying the encoding, maintenance, and retrieval phase in a delayed-match-to-sample task Habeck C; Rakitin BC; Moeller J; Scarmeas N; Zarahn E; Brown T; Stern Y Cognitive Brain Research 2005 15820629

An evoked auditory response fMRI study of the effects of rTMS on putative AVH pathways in healthy volunteers Tracy DK; O'Daly O; Joyce DW; Michalopoulou PG; Basit BB; Dhillon G; McLoughlin DM; Shergill SS Neuropsychologia 2010 19769994

An fMRI case report of photophobia: activation of the trigeminal nociceptive pathway Moulton EA; Becerra L; Borsook D Pain 2009 19674842

An fMRI investigation of syllable sequence production Bohland JW; Guenther FH NeuroImage 2006 16730195

An fMRI study of theory of mind in schizophrenic patients with “passivity” symptoms Brune M; Lissek S; Fuchs N; Witthaus H; Peters S; Nicolas V; Juckel G; Tegenthoff M Neuropsychologia 2008 18329671

Anterior cingulate cortex: An fMRI analysis of conflict specificity and functional differentiation Milham MP; Banich MT Human Brain Mapping 2005 15834861

Anticipating instrumentally obtained and passively-received rewards: a factorial fMRI investigation Bjork JM; Hommer DW Behavioural Brain Research 2007 17140674

Anticipation of novelty recruits reward system and hippocampus while promoting recollection Wittmann BC; Bunzeck N; Dolan RJ; Duzel E NeuroImage 2007 17764976

Are errors differentiable from deceptive responses when feigning memory impairment? An fMRI study Lee TM; Au RK; Liu HL; Ting KH; Huang CM; Chan CC Brain and Cognition 2009 18938008

Art for reward's sake: visual art recruits the ventral striatum Lacey S; Hagtvedt H; Patrick VM; Anderson A; Stilla R; Deshpande G; Hu X; Sato JR; Reddy S; Sathian K NeuroImage 2011 21111833

Auditory task presentation reveals predominantly right hemispheric fMRI activation patterns during mental calculation Fehr T; Code C; Herrmann M Neuroscience Letters 2008 18093736

Automatic brain response to facial emotion as a function of implicitly and explicitly measured extraversion Suslow T; Kugel H; Reber H; Bauer J; Dannlowski U; Kersting A; Arolt V; Heindel W; Ohrmann P; Egloff B Neuroscience 2010 20144695

Basal Ganglia Functional Connectivity Based on a Meta-Analysis of 126 Positron Emission Tomography and Functional Magnetic Resonance Imaging Publications Postuma RB; Dagher A Cerebral Cortex 2006 16373457

Beyond common resources: the cortical basis for resolving task interference Hester R; Murphy K; Garavan H NeuroImage 2004 15325367

BOLD correlates of trial-by-trial reaction time variability in gray and white matter: a multi-study fMRI analysis Yarkoni T; Barch DM; Gray JR; Conturo TE; Braver TS PLoS ONE 2009 19165335

Brain activation and hypothalamic functional connectivity during human non-rapid eye movement sleep: an EEG/fMRI study Kaufmann C; Wehrle R; Wetter TC; Holsboer F; Auer DP; Pollmacher T; Czisch M Brain 2006 16339798

Brain Activation during Anticipation of Sound Sequences Leaver AM; Van Lare J; Zielinski B; Halpern AR; Rauschecker JP Journal of Neuroscience 2009 19244522

Brain activation during execution and motor imagery of novel and skilled sequential hand movements Lacourse MG; Orr EL; Cramer SC; Cohen MJ NeuroImage 2005 16046149

Brain Activation during Input from Mechanoinsensitive versus Polymodal C-Nociceptors Ruehle BS; Handwerker HO; Lennerz JK; Ringler R; Forster C Journal of Neuroscience 2006 16707801

Brain activity associated with the electrodermal reactivity to acute heat pain Dube AA; Duquette M; Roy M; Lepore F; Duncan G; Rainville P NeuroImage 2009 19027077

Brain dynamics for perception of tactile allodynia (touch-induced pain) in postherpetic neuralgia Geha PY; Baliki MN; Wang X; Harden RN; Paice JA; Apkarian AV Pain 2008 18384958

Brain imaging of mechanically induced muscle versus cutaneous pain Uematsu H; Shibata M; Miyauchi S; Mashimo T Neuroscience Research 2011 21291923

Brain network dynamics during error commission Stevens MC; Kiehl KA; Pearlson GD; Calhoun VD Human Brain Mapping 2009 17979124

Brain networks for integrative rhythm formation Thaut MH; Demartin M; Sanes JN PLoS ONE 2008 18509462

Brain regions associated with the expression and contextual regulation of anxiety in primates Kalin NH; Shelton SE; Fox AS; Oakes TR; Davidson RJ Biological Psychiatry 2005 16043132

Brain Systems Mediating Cognitive Interference by Emotional Distraction Dolcos F; McCarthy G Journal of Neuroscience 2006 16481440

Cerebral activation during hypnotically induced and imagined pain Derbyshire SW; Whalley MG; Stenger VA; Oakley DA NeuroImage 2004 15325387

Cerebral blood flow changes induced by pedunculopontine nucleus stimulation in patients with advanced Parkinson's disease: A [15O] H2O PET study Ballanger B; Lozano AM; Moro E; van Eimeren T; Hamani C; Chen R; Cilia R; Houle S; Poon YY; Lang AE; Strafella AP Human Brain Mapping 2009 19479730

Cerebral regions processing first- and higher-order motion in an opposed-direction discrimination task European Journal of Neuroscience 2003

Changes in brain function and morphology in patients with recurring herpes simplex virus infections and chronic pain Vartiainen N; Kallio-Laine K; Hlushchuk Y; Kirveskari E; Seppanen M; Autti H; Jousmaki V; Forss N; Kalso E; Hari R Pain 2009 19446957

Changing channels: an fMRI study of aging and cross-modal attention shifts Townsend J; Adamo M; Haist F NeuroImage 2006 16549368

Clustered functional MRI of overt speech production Soros P; Sokoloff LG; Bose A; McIntosh AR; Graham SJ; Stuss DT NeuroImage 2006 16631384

Cocaine dependence and attention switching within and between verbal and visuospatial working memory Kubler A; Murphy K; Garavan H European Journal of Neuroscience 2005 15869491

Combined event-related fMRI and intracerebral ERP study of an auditory oddball task Brazdil M; Dobsik M; Mikl M; Hlustik P; Daniel P; Pazourkova M; Krupa P; Rektor I NeuroImage 2005 15862229

Common and distinct neural substrates for the perception of speech rhythm and intonation Zhang L; Shu H; Zhou F; Wang X; Li P Human Brain Mapping 2010 20063360

Common and unique components of inhibition and working memory: an fMRI, within-subjects investigation McNab F; Leroux G; Strand F; Thorell L; Bergman S; Klingberg T Neuropsychologia 2008 18573510

Common and unique components of response inhibition revealed by fMRI Wager TD; Sylvester CY; Lacey SC; Nee DE; Franklin M; Jonides J NeuroImage 2005 16019232

Common neural substrates for visual working memory and attention Mayer JS; Bittner RA; Nikolic D; Bledowski C; Goebel R; Linden DE NeuroImage 2007 17462914

Compassionate attitude towards others' suffering activates the mesolimbic neural system Kim JW; Kim SE; Kim JJ; Jeong B; Park CH; Son AR; Song JE; Ki SW Neuropsychologia 2009 19428038

Compensatory cortical activation observed by fMRI during a cognitive task at the earliest stage of multiple sclerosis Audoin B; Ibarrola D; Ranjeva JP; Confort-Gouny S; Malikova I; Ali-Cherif A; Pelletier J; Cozzone P Human Brain Mapping 2003 14505331

Compensatory mechanisms underlie intact task-switching performance in schizophrenia Jamadar S; Michie P; Karayanidis F Neuropsychologia 2010 20036266 COMT Val(108/158)Met polymorphism effects on emotional brain function and negativity bias Williams LM; Gatt JM; Grieve SM; Dobson-Stone C; Paul RH; Gordon E; Schofield PR NeuroImage 2010 20139013

Connectivity of the primate superior colliculus mapped by concurrent microstimulation and event-related FMRI Field CB; Johnston K; Gati JS; Menon RS; Everling S PLoS ONE 2008 19079541

Constrained principal component analysis reveals functionally connected load-dependent networks involved in multiple stages of working memory Metzak P; Feredoes E; Takane Y; Wang L; Weinstein S; Cairo T; Ngan ET; Woodward TS Human Brain Mapping 2010 20572208

Constructive episodic simulation of the future and the past: distinct subsystems of a core brain network mediate imagining and remembering Addis DR; Pan L; Vu MA; Laiser N; Schacter DL Neuropsychologia 2009 19041331

Cortical activation in response to pure taste stimuli during the physiological states of hunger and satiety Haase L; Cerf-Ducastel B; Murphy C NeuroImage 2009 19007893

Cortical activity in Parkinson's disease during executive processing depends on striatal involvement Monchi O; Petrides M; Mejia-Constain B; Strafella AP Brain 2007 17121746

Cortical and subcortical contributions to saccade latency in the human brain Neggers SF; Raemaekers MA; Lampmann EE; Postma A; Ramsey NF European Journal of Neuroscience 2005 15926933

Cortical dysfunction in patients with Huntington's disease during working memory performance Wolf RC; Vasic N; Schonfeldt-Lecuona C; Ecker D; Landwehrmeyer GB Human Brain Mapping 2009 18172852

Cortical effects of anticipation and endogenous modulation of visceral pain assessed by functional brain MRI in irritable bowel syndrome patients and healthy controls Song GH; Venkatraman V; Ho KY; Chee MW; Yeoh KG; Wilder-Smith CH Pain 2006 16846694

Cortical metabolic changes in the cerebellar variant of multiple system atrophy: a voxel-based FDG-PET study in 41 patients Lee PH; An YS; Yong SW; Yoon SN NeuroImage 2008 18203624

Cortical processing of visceral and somatic stimulation: differentiating pain intensity from unpleasantness Dunckley P; Wise RG; Aziz Q; Painter D; Brooks J; Tracey I; Chang L Neuroscience 2005 15896917

Creating a population-averaged standard brain template for Japanese macaques (M. fuscata) Quallo MM; Price CJ; Ueno K; Asamizuya T; Cheng K; Lemon RN; Iriki A NeuroImage 2010 20452439

Detection of unexpected events during spatial navigation in humans: bottom-up attentional system and neural mechanisms Iaria G; Fox CJ; Chen JK; Petrides M; Barton JJ European Journal of Neuroscience 2008 18279364 Developmental Changes in Human Cerebral Functional Organization for Word Generation Brown TT; Lugar HM; Coalson RS; Miezin FM; Petersen SE; Schlaggar BL Cerebral Cortex 2005 15297366

Differential cerebral activation during observation of expressive gestures and motor acts Lotze M; Heymans U; Birbaumer N; Veit R; Erb M; Flor H; Halsband U Neuropsychologia 2006 16730755

Differential cingulate and caudate activation following unexpected nonrewarding stimuli Davidson MC; Horvitz JC; Tottenham N; Fossella JA; Watts R; Ulug AM; Casey BJ NeuroImage 2004 15528104

Diminished neural sensitivity to irregular facial expression in first-episode schizophrenia Bleich-Cohen M; Strous RD; Even R; Rotshtein P; Yovel G; Iancu I; Olmer A; Hendler T Human Brain Mapping 2009 19172653

Discriminating imagined from perceived information engages brain areas implicated in schizophrenia Simons JS; Davis SW; Gilbert SJ; Frith CD; Burgess PW NeuroImage 2006 16797186

Dissection of perceptual, motor and autonomic components of brain activity evoked by noxious stimulation Piche M; Arsenault M; Rainville P Pain 2010 20417032

Dissociable processes of cognitive control during error and non-error conflicts: a study of the stop signal task Hendrick OM; Ide JS; Luo X; Li CS PLoS ONE 2010 20949134

Dissociable Roles for the Hippocampus and the Amygdala in Human Cued versus Context Fear Conditioning Marschner A; Kalisch R; Vervliet B; Vansteenwegen D; Buchel C Journal of Neuroscience 2008 18768697

Dissociable roles of medial orbitofrontal cortex in human operant extinction learning Finger EC; Mitchell DG; Jones M; Blair RJ NeuroImage 2008 18793731

Dissociating the contributions of independent corticostriatal systems to visual categorization learning through the use of reinforcement learning modeling and Granger causality modeling Seger CA; Peterson EJ; Cincotta CM; Lopez-Paniagua D; Anderson CW NeuroImage 2010 19969091

Distinct brain networks for time-varied characteristics of acupuncture Liu J; Qin W; Guo Q; Sun J; Yuan K; Liu P; Zhang Y; von Deneen KM; Liu Y; Tian J Neuroscience Letters 2010 19914337

Distinct striatal regions for planning and executing novel and automated movement sequences Jankowski J; Scheef L; Huppe C; Boecker H NeuroImage 2009 19059350

Distinction between the literal and intended meanings of sentences: A functional magnetic resonance imaging study of metaphor and sarcasm Uchiyama HT; Saito DN; Tanabe HC; Harada T; Seki A; Ohno K; Koeda T; Sadato N Cortex 2011 21333979

Dominance for Vestibular Cortical Function in the Non-dominant Hemisphere Cerebral Cortex 2003 12902399 Dopamine transporter gene variation modulates activation of striatum in youth with ADHD Bedard AC; Schulz KP; Cook EH Jr; Fan J; Clerkin SM; Ivanov I; Halperin JM; Newcorn JH NeuroImage 2010 20026227

Dorsolateral prefrontal cortex activity predicts responsiveness to cognitive-behavioral therapy in schizophrenia Kumari V; Peters ER; Fannon D; Antonova E; Premkumar P; Anilkumar AP; Williams SC; Kuipers E Biological Psychiatry 2009 19560121

Dynamic EEG-informed fMRI modeling of the pain matrix using 20-ms root mean square segments Brinkmeyer J; Mobascher A; Warbrick T; Musso F; Wittsack HJ; Saleh A; Schnitzler A; Winterer G Human Brain Mapping 2010 20162596

Dynamics of Prefrontal and Cingulate Activity during a Reward-Based Logical Deduction Task Landmann C; Dehaene S; Pappata S; Jobert A; Bottlaender M; Roumenov D; Le Bihan D Cerebral Cortex 2007 16707739

Dysfunction of reward processing correlates with alcohol craving in detoxified alcoholics Wrase J; Schlagenhauf F; Kienast T; Wustenberg T; Bermpohl F; Kahnt T; Beck A; Strohle A; Juckel G; Knutson B; Heinz A NeuroImage 2007 17291784

Dysfunction of ventral striatal reward prediction in schizophrenia Juckel G; Schlagenhauf F; Koslowski M; Wustenberg T; Villringer A; Knutson B; Wrase J; Heinz A NeuroImage 2006 16139525

Effect of menstrual cycle phase on corticolimbic brain activation by visual food cues Frank TC; Kim GL; Krzemien A; Van Vugt DA Brain Research 2010 20920491

Effects of aging on functional connectivity of the amygdala during negative evaluation: a network analysis of fMRI data St Jacques P; Dolcos F; Cabeza R Neurobiology of Aging 2010 18455837

Effects of aging on mindreading ability through the eyes: an fMRI study Castelli I; Baglio F; Blasi V; Alberoni M; Falini A; Liverta-Sempio O; Nemni R; Marchetti A Neuropsychologia 2010 20457166

Effects of Attention and Emotion on Repetition Priming and Their Modulation by Cholinergic Enhancement Bentley P; Vuilleumier P; Thiel CM; Driver J; Dolan RJ Journal of Neurophysiology 2003 12649315

Effort-Based Cost-Benefit Valuation and the Human Brain Croxson PL; Walton ME; O'Reilly JX; Behrens TE; Rushworth MF Journal of Neuroscience 2009 19357278

Emotional and autonomic consequences of spinal cord injury explored using functional brain imaging Nicotra A; Critchley HD; Mathias CJ; Dolan RJ Brain 2006 16330503

Emotional priming effects during Stroop task performance Hart SJ; Green SR; Casp M; Belger A NeuroImage 2010 19883772

Enhanced visual processing contributes to matrix reasoning in autism Soulieres I; Dawson M; Samson F; Barbeau EB; Sahyoun CP; Strangman GE; Zeffiro TA; Mottron L Human Brain Mapping 2009 19530215

Erotic and disgust-inducing pictures–differences in the hemodynamic responses of the brain Stark R; Schienle A; Girod C; Walter B; Kirsch P; Blecker C; Ott U; Schafer A; Sammer G; Zimmermann M; Vaitl D Biological Psychology 2005 16038771

Event-related fMRI studies of episodic encoding and retrieval: meta-analyses using activation likelihood estimation Spaniol J; Davidson PS; Kim AS; Han H; Moscovitch M; Grady CL Neuropsychologia 2009 19428409

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