Efferent connections of the rostral linear nucleus of the ventral tegmental area in the rat

Del-Fava, F.; Hasue, R.H.; Ferreira, J.G.P.; Shammah-Lagnado, S.J.

doi:10.1016/j.neuroscience.2006.12.039

Cited by 56Neurotransmitter Receptor Influence on BehaviorNeuroscience and Neuropharmacology ResearchNeural and Behavioral Psychology Studies

Efferent connections of the rostral linear nucleus of the ventral tegmental area in the rat

Del-Fava, F., Hasue, R.H., Ferreira, J.G.P., Shammah-Lagnado, S.J.·2007·Neuroscience

DOI 10.1016/j.neuroscience.2006.12.039

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Abstract

The ventral tegmental area (VTA) is crucially involved in brain reward, motivated behaviors, and drug addiction. This district is functionally heterogeneous, and studying the connections of its different parts may contribute to clarify the structural basis of intra-VTA functional specializations. Here, the efferents of the rostral linear nucleus (RLi), a midline VTA component, were traced in rats with the Phaseolus vulgaris leucoagglutinin (PHA-L) technique. The results show that the RLi heavily innervates the olfactory tubercle (mainly the polymorph layer) and the ventrolateral part of the ventral pallidum, but largely avoids the accumbens. The RLi also sends substantial projections to the magnocellular preoptic nucleus, lateral hypothalamus, central division of the mediodorsal thalamic nucleus, lateral part of the lateral habenula and supraoculomotor region, and light projections to the prefrontal cortex, basolateral amygdala, and dorsal raphe nucleus. A similar set of projections was observed after injections in rostromedial VTA districts adjacent to RLi, but these districts also send major outputs to the lateral ventral striatum. Overall, the data suggest that the RLi is a distinct VTA component in that it projects primarily to pallidal regions of the olfactory tubercle and to their diencephalic targets, the central division of the mediodorsal thalamic nucleus and the lateral part of the lateral habenula. Because the rat RLi reportedly contains a lower density of dopaminergic neurons as compared with most of the VTA, its unusual projections may reflect a non-dopaminergic, putative GABAergic, phenotype, and this distinctive cell population seemingly extends beyond RLi boundaries into the laterally adjacent VTA. By being connected to the central division of the mediodorsal thalamic nucleus (directly and via ventral striatopallidal system) and to the magnocellular preoptic nucleus, the RLi and its surroundings may play a role in olfactory-guided behaviors, which are part of the approach responses associated with appetitive motivational states.

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Recent anterograde-tracer data suggest that neurons in the rostral linear nucleus project to the pallidal zone of the tubercle.
“Although it is not demonstrated by the data presented here, recent anterograde-tracer data suggest that neurons in this structure projects to the pallidal zone of the tubercle”
From Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex (2007) · cites this paper as Del-Fava et al., 2007
Dopamine neurons in the central linear nucleus selectively project to the ventromedial striatum.
“Similarly, dopamine neurons in the central linear nucleus selectively project to the ventromedial striatum, connectivity that is consistent with recent data obtained with the anterograde tracer PHA-L”
From Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex (2007) · cites this paper as Del-Fava et al., 2007
FG labeling found in the rostral linear nucleus and parafasciculus retroflexus area after FG deposits in the olfactory tubercle most likely resulted from the projection to the pallidal, but not striatal, zone of the olfactory tubercle.
“In addition, FG labeling found in the rostral linear nucleus and parafasciculus retroflexus area after FG deposits in the olfactory tubercle most likely resulted from the projection to the pallidal, but not striatal, zone of the olfactory tubercle; recent PHA-L data suggest that neurons in the rostral linear nucleus and parafasciculus retroflexus area project to the pallidal zone (Del-Fava et al.,”
From Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex (2007) · cites this paper as Del-Fava et al., 2007

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Zahm, D. S., Záborszky, L., Alheid, G. F., & Heimer, L. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902550410 · Cited by 108 · see citing works
Dopamine neurones of the ventral tegmentum project to both medial and lateral habenula
Phillipson, O. T., & PYCOCK, C. (1982) · Experimental Brain Research · doi:10.1007/bf00235766 · Cited by 107 · see citing works
Role of Mediodorsal Thalamic Nucleus in Olfactory Discrimination Learning in Rats
Slotnick, B. M., & Kaneko, N. (1981) · Science · doi:10.1126/science.7280684 · Cited by 106 · see citing works
Afferent connections of the interstitial nucleus of the posterior limb of the anterior commissure and adjacent amygdalostriatal transition area in the rat
Shammah‐Lagnado, S. J., Alheid, G. F., & Heimer, L. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)90280-4 · Cited by 106 · see citing works
Regional Differences Within the Rat Ventral Tegmental Area for Muscimol Self-Infusions
Ikemoto, S., Murphy, J. M., & McBride, W. J. H. (1998) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(98)00086-0 · Cited by 104 · see citing works
Origin, course and termination of the mesohabenular dopamine pathway in the rat
Skagerberg, G., Lindvall, O., & Björklund, A. (1984) · Brain Research · doi:10.1016/0006-8993(84)90465-7 · Cited by 100 · see citing works
Distinct sites of opiate reward and aversion within the midbrain identified using a herpes simplex virus vector expressing GluR1
Carlezon, W. A., Haile, C. N., Coppersmith, R., Hayashi, Y., Malinow, R., Neve, R. L., & Nestler, E. J. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-05-j0002.2000 · Cited by 98 · see citing works
Interconnections between the primate cerebellum and midbrain near‐response regions
May, P. J., Porter, J. D., & Gamlin, P. D. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903150108 · Cited by 96 · see citing works
Increased Mesolimbic GABA Concentration Blocks Heroin Self-Administration in the Rat
Xi, Z., & Stein, E. A. (2000) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)39113-x · Cited by 95 · see citing works
Olfactory system activation from sniffing: effects in piriform and orbitofrontal cortex
Kareken, D. A., Sabri, M., Radnovich, A. J., Claus, E. D., FORESMAN, B. H., Hector, D. H., & Hutchins, G. D. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.01.008 · Cited by 89 · see citing works
Simulation of the classically conditioned nictitating membrane response by a neuron-like adaptive element: Response topography, neuronal firing, and interstimulus intervals
Moore, J. W., Desmond, J. E., Berthier, N. E., Blazis, D. E. J., Sutton, R. S., & Barto, A. G. (1986) · Behavioural Brain Research · doi:10.1016/0166-4328(86)90092-6 · Cited by 86 · see citing works
Sources of presumptive glutamatergic/aspartatergic afferents to the mediodorsal nucleus of the thalamus in the rat
Ray, J. P., Russchen, F. T., Fuller, T. A., & Price, J. L. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903200403 · Cited by 85 · see citing works
Projections from the ventral tegmental area and mesencephalic raphe to the dorsal raphe nucleus in the rat
Kal�n, P., Skagerberg, G., & Lindvall, O. (1988) · Experimental Brain Research · doi:10.1007/bf00279662 · Cited by 81 · see citing works
Distribution of dopamine-immunoreactive fibers in the rat brainstem
Kitahama, K., Nagatsu, I., Geffard, M., & Maeda, T. (2000) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(99)00047-2 · Cited by 79 · see citing works
The central extended amygdala network as a proposed circuit underlying reward valuation
Waraczynski, M. A. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.09.001 · Cited by 75 · see citing works
Ventral pallidum self-stimulation: a moveable electrode mapping study
Panagis, G., Miliaressis, E., Anagnostakis, Y., & Spyraki, C. (1995) · Behavioural Brain Research · doi:10.1016/0166-4328(94)00169-g · Cited by 75 · see citing works
Responses of ventral tegmental area GABA neurons to brain stimulation reward
Steffensen, S. C., Lee, R., Stobbs, S. H., & Henriksen, S. J. (2001) · Brain Research · doi:10.1016/s0006-8993(01)02581-1 · Cited by 68 · see citing works
Origin of the dopaminergic innervation of the rat dorsal raphe nucleus
Peyron, C., Luppi, P., Kitahama, K., Fort, P., Hermann, D. M., & Jouvet, M. (1995) · Neuroreport · doi:10.1097/00001756-199512150-00019 · Cited by 67 · see citing works
The neurones of origin for the mesohabenular dopamine pathway
Phillipson, O. T., & Griffith, A. C. (1980) · Brain Research · doi:10.1016/0006-8993(80)90447-3 · Cited by 64 · see citing works
Targeting of serotonin 1a receptors to dopaminergic neurons within the parabrachial subdivision of the ventral tegmental area in rat brain
Doherty, M. D., & Pickel, V. M. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1147 · Cited by 63 · see citing works
Role for Dopamine Neurons of the Rostral Linear Nucleus and Periaqueductal Gray in the Rewarding and Sensitizing Properties of Heroin
Flores, J. A., Galán-Rodríguez, B., Ramiro-Fuentes, S., & Fernández‐Espejo, E. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300946 · Cited by 62 · see citing works
The ventral striatopallidothalamic projection. III. Striatal cells of the olfactory tubercle establish direct synaptic contact with ventral pallidal cells projecting to mediodorsal thalamus
Zahm, D. S., & Heimer, L. (1987) · Brain Research · doi:10.1016/0006-8993(87)91388-6 · Cited by 57 · see citing works
Effect of amphetamine on extrastriatal D2 dopamine receptor binding in the primate brain: A PET study
Chou, Y.-H., Halldin, C., & Farde, L. (2000) · Synapse · doi:10.1002/1098-2396(200011)38:2 · Cited by 57 · see citing works
The origin of the annulo-olivary tract with notes on other mesencephalo-olivary pathways. A study by the horseradish peroxidase method
Henkel, C. K., Linauts, M., & Martin, G. F. (1975) · Brain Research · doi:10.1016/0006-8993(75)90250-4 · Cited by 56 · see citing works
Widespread cortical projections of the ventral tegmental area and of other brain stem structures in the cat
Maragkowitsch, H. J., & Irle, E. (1981) · Experimental Brain Research · doi:10.1007/bf00238880 · Cited by 54 · see citing works
Intravenous heroin self‐administration decreases GABA efflux in the ventral pallidum: an in vivo microdialysis study in rats
Caillé, S., & Parsons, L. H. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03497.x · Cited by 48 · see citing works
Region‐specific targeting of dopamine D2‐receptors and somatodendritic vesicular monoamine transporter 2 (VMAT2) within ventral tegmental area subdivisions
Pickel, V. M., Chan, J., & Nirenberg, M. J. (2002) · Synapse · doi:10.1002/syn.10092 · Cited by 47 · see citing works
The relationship between self-stimulation and sniffing in rats: does a common brain system mediate these behaviors?
Ikemoto, S., & Panksepp, J. (1994) · Behavioural Brain Research · doi:10.1016/0166-4328(94)90155-4 · Cited by 46 · see citing works
Cholecystokinin and neurotensin mRNAs are differentially expressed in subnuclei of the ventral tegmental area
Jayaraman, A., Nishimori, T., Dobner, P. R., & Uhl, G. R. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902960209 · Cited by 41 · see citing works
The tectorecipient zone in the inferior olivary nucleus in the rat
Akaike, T. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903200311 · Cited by 39 · see citing works
Ventromedial mesencephalic tegmental (VMT) projections to ten functionally different cortical areas in the cat: Topography and quantitative analysis
Scheibner, T., & Törk, I. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902590206 · Cited by 32 · see citing works
Lesions in the magnocellular preoptic nucleus decrease olfactory investigation in rats
Paolini, A. G., & McKenzie, J. S. (1996) · Behavioural Brain Research · doi:10.1016/s0166-4328(96)89082-6 · Cited by 27 · see citing works
Organization of afferent connections of the feline lateral habenular nucleus
McBride, R. L. (1981) · The Journal of Comparative Neurology · doi:10.1002/cne.901980109 · Cited by 26 · see citing works
Distinct populations of neurons in the ventromedial periaqueductal gray project to the rostral ventral medulla and abducens nucleus
Bockstaele, E. J. V., & Aston‐Jones, G. (1992) · Brain Research · doi:10.1016/0006-8993(92)90609-d · Cited by 24 · see citing works
Intracellular recording of magnocellular preoptic neuron responses to olfactory brain
Paolini, A. G., & McKenzie, J. S. (1997) · Neuroscience · doi:10.1016/s0306-4522(96)00566-0 · Cited by 16 · see citing works

Flagged first, then by citations

3 of the 124 references couldn’t be matched to a known paper.

Sorted by citations

Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex
Ikemoto, S. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.05.004 · Cited by 1,477 · see citing works
Cortico-Basal Ganglia Reward Network: Microcircuitry
Sesack, S. R., & Grace, A. A. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.93 · Cited by 985 · see citing works
“The majority of projections from the rostral linear nucleus appear to be non-dopaminergic (Swanson, 1982; Del-Fava et al, 2007).”
Influential
The ventral pallidum: Subregion-specific functional anatomy and roles in motivated behaviors
Root, D. H., Meléndez, R. I., Záborszky, L., & Napier, T. C. (2015) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.03.005 · Cited by 343 · see citing works
GABAergic and glutamatergic efferents of the mouse ventral tegmental area
Taylor, S. R., Badurek, S., Dileone, R., Nashmi, R., Minichiello, L., & Picciotto, M. R. (2014) · The Journal of Comparative Neurology · doi:10.1002/cne.23603 · Cited by 209 · see citing works
“The DAergic projections in this study are largely consistent with prior work in rat (Swanson, 1982; Klitenick et al., 1992; Del-Fava et al., 2007).”
Result
Sniffing out the contributions of the olfactory tubercle to the sense of smell: Hedonics, sensory integration, and more?
Wesson, D. W., & Wilson, D. A. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.08.004 · Cited by 208 · see citing works
An update on the connections of the ventral mesencephalic dopaminergic complex
Yetnikoff, L., Lavezzi, H. N., Reichard, R. A., & Zahm, D. S. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.04.010 · Cited by 172 · see citing works
“Contrary to expectations, projections from GPb to the LHb are excitatory (Shabel et al., 2012; Hong and Hikosaka; 2013).”
BackgroundInfluential
The Lateral Habenula:No Longer Neglected
Geisler, S., & Trimble, M. (2008) · CNS Spectrums · doi:10.1017/s1092852900016710 · Cited by 149 · see citing works
“Fibers originating in the GPi arborize extensively in the LHb, and exhibit numerous terminal-like specializations consistent with an important pallidal influence on lateral habenular functions.(61) Indeed, the LHb is the most densely innervated target of the GPi.”
Background
Long-range projection neurons of the mouse ventral tegmental area: a single-cell axon tracing analysis
Aransay, A., Rodríguez-López, C., García‐Amado, M., Clascá, F., & Prensa, L. (2015) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2015.00059 · Cited by 143 · see citing works
Organization of ventral tegmental area projections to the ventral tegmental area–nigral complex in the rat
Ferreira, J. G. P., Del-Fava, F., Hasue, R. H., & Shammah‐Lagnado, S. J. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.02.003 · Cited by 101 · see citing works
Central olfactory structures
Cleland, T. A., & Linster, C. (2019) · Handbook of clinical neurology · doi:10.1016/b978-0-444-63855-7.00006-x · Cited by 97 · see citing works
Connections of the lateral hypothalamic area juxtadorsomedial region in the male rat
Hahn, J. D., & Swanson, L. W. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23064 · Cited by 87 · see citing works
“Previous pathway-tracing studies have investigated VTA connections extensively by using current (Swanson, 1982; Geisler and Zahm, 2005; Del-Fava et al., 2007; Ikemoto, 2007; Ferreira et al., 2008; Kaufling et al., 2009), and prior (Phillipson, 1979; Beckstead et al., 1979; Oades and Halliday, 1987)…”
Method
Review of the cytology and connections of the lateral habenula, an avatar of adaptive behaving
Zahm, D. S., & Root, D. H. (2017) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.06.004 · Cited by 91 · see citing works
“The LHb neurotransmission plot thickens further upon consideration of the larger, non-THexpressing mesohabenular projection (Swanson, 1982; Del-Fava et al., 2007).”
Background
Dopaminergic projections from the VTA substantially contribute to the mesohabenular pathway in the rat
Gruber, C., Kahl, A., Lebenheim, L., Kowski, A. B., Dittgen, A., & Veh, R. W. (2007) · Neuroscience Letters · doi:10.1016/j.neulet.2007.09.016 · Cited by 85 · see citing works
Habenular connections with the dopaminergic and serotonergic system and their role in stress‐related psychiatric disorders
Metzger, M., Souza, R., Lima, L. B., Bueno, D., Gonçalves, L., Sego, C., Donato, J., & Shammah‐Lagnado, S. J. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14647 · Cited by 77 · see citing works
“Thus, both rostrodorsomedial PBP and RLi have been described to preferentially project to (Del-Fava et al., 2007) and get input from (Petzel et al.”
Background
Projections from the rat pedunculopontine and laterodorsal tegmental nuclei to the anterior thalamus and ventral tegmental area arise from largely separate populations of neurons
Holmstrand, E. C., & Sesack, S. R. (2011) · Brain Structure and Function · doi:10.1007/s00429-011-0320-2 · Cited by 70 · see citing works
“Strikingly, RLi neurons project only meagerly, or not at all, to classical VTA targets such as the nucleus accumbens and prefrontal cortex (Del-Fava et al. 2007).”
Ventral pallidum DRD3 potentiates a pallido-habenular circuit driving accumbal dopamine release and cocaine seeking
Pribiag, H., Shin, S., Wang, E. H.-J., Sun, F., Datta, P., Okamoto, A., Guss, H., Jain, A., Wang, X.-Y., Freitas, B. D., et al. (2021) · Neuron · doi:10.1016/j.neuron.2021.05.002 · Cited by 63 · see citing works
“, 2011) and receives DAergic innervation from the VTA (Del-Fava et al., 2007; Klitenick et al., 1992; Taylor et al., 2014).”
Inputs to the midbrain dopaminergic complex in the rat, with emphasis on extended amygdala‐recipient sectors
Zahm, D. S., Cheng, A. Y., Lee, T. J., Ghobadi, C. W., Schwartz, Z. M., Geisler, S., Parsely, K. P., Gruber, C., & Veh, R. W. (2011) · The Journal of Comparative Neurology · doi:10.1002/cne.22670 · Cited by 65 · see citing works
A subset of ventral tegmental area dopamine neurons responds to acute ethanol
Mrejeru, A., Martí‐Prats, L., Avegno, E. M., Harrison, N. L., & Sulzer, D. L. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2014.12.081 · Cited by 54 · see citing works
“Distinct subnuclei within the VTA have been described by immunostaining and are readily identifiable (Del-Fava et al., 2007; Ferreira et al., 2008; Fu et al., 2012).”
Background
Olfactory tubercle stimulation alters odor preference behavior and recruits forebrain reward and motivational centers
FitzGerald, B. J., Richardson, K., & Wesson, D. W. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00081 · Cited by 51 · see citing works
“Likely analyzing additional brain structures, especially the ventral tegmental area and orbitofrontal cortex, would provide additional evidence for the functional interconnectedness of the OT (Barbas, 1993; Illig, 2005; Del-Fava et al., 2007).”
Neurotensin in the Ventral Pallidum Increases Extracellular γ-Aminobutyric Acid and Differentially Affects Cue- and Cocaine-Primed Reinstatement
Torregrossa, M. M., & Kalivas, P. W. (2008) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.107.130310 · Cited by 49 · see citing works
“However, GABA may also be released from VTA projection neurons (Del-Fava et al., 2007) or from recurrent collaterals within the VP itself.”
Background
The Neural Representation of Goal-Directed Actions and Outcomes in the Ventral Striatum's Olfactory Tubercle
Gadziola, M. A., & Wesson, D. W. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.3328-15.2016 · Cited by 47 · see citing works
The Distinct Functions of Dopaminergic Receptors on Pain Modulation: A Narrative Review
Wang, X., Mokhtari, T., Zeng, Y., Yue, L., & Hu, L. (2021) · Neural Plasticity · doi:10.1155/2021/6682275 · Cited by 45 · see citing works
“Noxious footshocks are believed to inhibit the activities of DA neurons in the dorsal VTA, but physically excite the activities of DA neurons in the ventral VTA, suggesting that VTA DA neurons are heterogeneous in the processing of rewarding and aversive events [63].”
Background
A discrete dopaminergic projection from the incertohypothalamic A13 cell group to the dorsolateral periaqueductal gray in rat
Messanvi, F., Eggens‐Meijer, E., Roozendaal, B., & van der Want, J. J. L. (2013) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2013.00041 · Cited by 42 · see citing works
Diverse midbrain dopaminergic neuron subtypes and implications for complex clinical symptoms of Parkinson’s disease
Carmichael, K., Sullivan, B. T., Lopez, E., Sun, L., & Cai, H. (2021) · Ageing and Neurodegenerative Diseases · doi:10.20517/and.2021.07 · Cited by 46 · see citing works
Midbrain
Puelles, E., Martı́nez-de-la-Torre, M., WATSON, C. R. R., & Puelles, L. (2011) · Elsevier eBooks · doi:10.1016/b978-0-12-369497-3.10010-x · Cited by 37 · see citing works
Neurochemical organization of the ventral striatum’s olfactory tubercle
Cansler, H. L., Wright, K. N., Stetzik, L. A., & Wesson, D. W. (2019) · Journal of Neurochemistry · doi:10.1111/jnc.14919 · Cited by 34 · see citing works
Regulation of Energy Balance and Body Weight by the Brain: A Distributed System Prone to Disruption
Faulconbridge, L. F., & Hayes, M. R. (2011) · Psychiatric Clinics of North America · doi:10.1016/j.psc.2011.08.008 · Cited by 33 · see citing works
The Mesoaccumbens Pathway: A Retrograde Labeling and Single-Cell Axon Tracing Analysis in the Mouse
Rodríguez-López, C., Clascá, F., & Prensa, L. (2017) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2017.00025 · Cited by 31 · see citing works
“The few available anterograde-tracing studies were carried out with low-sensitivity methods in rats (Fallon and Moore, 1978; Beckstead et al., 1979).”
Method
Anterior and posterior parts of the rat ventral tegmental area and the rostromedial tegmental nucleus receive topographically distinct afferents from the lateral habenular complex
Petzel, A., Bernard, R., Poller, W. C., & Veh, R. W. (2017) · The Journal of Comparative Neurology · doi:10.1002/cne.24200 · Cited by 31 · see citing works
“In turn, efferent projections from the ventral aVTA are known to target the LHbM (Del-Fava et al., 2007; Goncalves et al., 2012; Gruber et al., 2007).”
Background
nNOS-Expressing Neurons in the Ventral Tegmental Area and Substantia Nigra Pars Compacta
Paul, E. J., Kalk, E., Tossell, K., Irvine, E. E., Franks, N. P., Wisden, W., Withers, D. J., LEIPER, J. M., & Ungless, M. A. (2018) · eNeuro · doi:10.1523/eneuro.0381-18.2018 · Cited by 31 · see citing works
“All of these regions are known to receive input from the RLi (Del-Fava et al., 2007).”
BackgroundMethodResultInfluential
Increased Perioculomotor Urocortin 1 Immunoreactivity in Genetically Selected Alcohol Preferring Rats
Chamine, I., Spangler, E., Cannella, N., Sabino, V., Cottone, P., Ciccocioppo, R., Zorrilla, E. P., & Ryabinin, A. E. (2009) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2009.01033.x · Cited by 31 · see citing works
“Interestingly, tracing studies indicate that the shell of nucleus accumbens in rats is heavily innervated by the TH neurons of the rostral linear nucleus, including neurons in the vicinity of pIII (Del-Fava et al., 2007; Hasue and Shammah-Lagnado, 2002).”
Background
Chronic 13-cis-retinoic acid administration disrupts network interactions between the raphe nuclei and the hippocampal system in young adult mice
O’Reilly, K. C., Shumake, J., Bailey, S., Gonzalez-Lima, F., & Lane, M. A. (2009) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2008.12.037 · Cited by 28 · see citing works
Statistical modeling implicates neuroanatomical circuit mediating stress relief by ‘comfort’ food
Ulrich‐Lai, Y. M., Christiansen, A. M., Wang, X., Song, S., & Herman, J. P. (2015) · Brain Structure and Function · doi:10.1007/s00429-015-1092-x · Cited by 26 · see citing works
“, via intervening synapses in the lateral hypothalamus or ventral tegmental area) (Hosoya and Matsushita 1980; Heimer et al. 1991; Kirouac and Ganguly 1995; Usuda et al. 1998; Del-Fava et al. 2007; Schmitt et al. 2012).”
Background
Top-down projections of the prefrontal cortex to the ventral tegmental area, laterodorsal tegmental nucleus, and median raphe nucleus
Souza, R., Bueno, D., Lima, L. B., Muchon, M. J., Gonçalves, L., Donato, J., Shammah‐Lagnado, S. J., & Metzger, M. (2022) · Brain Structure and Function · doi:10.1007/s00429-022-02538-2 · Cited by 27 · see citing works
In vivo structural connectome of arousal and motor brainstem nuclei by 7 Tesla and 3 Tesla MRI
García‐Gomar, M. G., Singh, K., Cauzzo, S., & Bianciardi, M. (2022) · Human Brain Mapping · doi:10.1002/hbm.25962 · Cited by 23 · see citing works
“Previous invasive research in rodents showed anatomical connectivity of RLi with the striatum (strongly with the pallidum), hypothalamus, thalamus, prefrontal cortex, DR, and amygdala (Del-Fava et al., 2007), although its”
Background
Neural circuits provide insights into reward and aversion
Chen, W. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2022.1002485 · Cited by 22 · see citing works
“The lateral VTA is projected to the VPr, VPvm, VPdl, and VPvl, and the midline VTA is projected to the medial part of the VP (Groenewegen et al., 1993; Del-Fava et al., 2007; Taylor et al., 2014).”
Method
TheFoxb1‐expressing neurons of the ventrolateral hypothalamic parvafox nucleus project to defensive circuits
Bilella, A., Álvarez-Bolado, G., & Celio, M. R. (2016) · The Journal of Comparative Neurology · doi:10.1002/cne.24057 · Cited by 23 · see citing works
Leptin action in the midbrain: From reward to stress
Xu, L. (2014) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2014.06.007 · Cited by 20 · see citing works
“The RLi nucleus in the midbrain is composed of small and roundish DA neurons, and some authors have considered it as independent from the VTA (e.g. Phillipson, 1979; Swanson, 1982) while others have not (Oades and Halliday, 1987; Del-Fava et al., 2007).”
Background
Heroin-induced conditioned immunomodulation requires expression of IL-1β in the dorsal hippocampus
Szczytkowski, J. L., Lebonville, C. L., Hutson, L. W., Fuchs, R. A., & Lysle, D. T. (2013) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2013.01.076 · Cited by 13 · see citing works
“These brain regions are extensively connected to one another and to the DH, providing anatomical basis for a putative neural circuitry (Del-Fava et al., 2007; Ikemoto, 2007; Mcdonald, 1991).”
Background
Mere exposure: Preference change for novel drinks reflected in human ventral tegmental area
Ballard, I. C., Hennigan, K., & McClure, S. M. (2017) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_01098 · Cited by 10 · see citing works
Nuclear organization of the serotonergic system in the brain of the rock cavy (Kerodon rupestris)
Soares, J. G., Cavalcanti, J. R. L. D. P., Oliveira, F. G., de Pontes, A. L. B., de Sousa, T. B., de Freitas, L. M., Cavalcante, J. S., do Nascimento, E. S., Cavalcante, J. C., & Costa, M. S. M. O. (2012) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2012.03.001 · Cited by 11 · see citing works
Ascending Activating Systems of the Brain for Emotional Arousal
Brudzyński, S. M., Silkstone, M., & Mulvihill, K. G. (2018) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-809600-0.00023-8 · Cited by 6 · see citing works
Localization of stereotaxic coordinates for the ventral tegmental area in early adolescent, mid-adolescent and adult rats
Sponaugle, A. E., Badanich, K. A., & Kirstein, C. L. (2008) · Brain Research · doi:10.1016/j.brainres.2008.04.060 · Cited by 2 · see citing works
Thyrotropin-releasing hormone and dopaminergic systems interact in the ventral tegmental area to regulate food intake in rats
Srivastava, A., Waghade, A. M., Sahoo, D., Divyajyoti, S., Patil, A., Chattopadhyay, A., Kokare, D. M., & Singru, P. S. (2026) · Neuropharmacology · doi:10.1016/j.neuropharm.2026.111091 · Cited by 1 · see citing works
Role of Prefrontal Cortex Dopamine and Noradrenaline Circuitry in Addiction
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Authors: Del-Fava, F., Hasue, R. H., Ferreira, J. G. P., & Shammah-Lagnado, S. J.
Affiliations: Universidade de São Paulo (BR)
ORCID: Hasue, R.H.
Ferreira, J.G.P.
Venue: Neuroscience
Publisher: Elsevier BV
Published: 2007-03
Volume: 145
Issue: 3
Pages: 1059-1076
ISSN: 0306-4522 (ISSN-L)
DOI: 10.1016/j.neuroscience.2006.12.039
OpenAlex: W1986446339
Cited by: 56
References: 124
Citations by year: 2026: 1 · 2025: 1 · 2024: 1 · 2022: 4 · 2021: 3 · 2019: 4 · 2018: 2 · 2017: 4 · 2016: 5 · 2015: 5 · 2014: 5 · 2013: 3 · 2012: 3
FWCI: 1.45
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Neuroscience (publishedVersion)
PubMed (publishedVersion)
Funders: Fundação de Amparo à Pesquisa do Estado de São Paulo (02/07014-2, 03/07239-7, 05/51607-6)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Keywords: ventral tegmental area, efferent projections, olfactory tubercle, ventral pallidum, mediodorsal thalamus, lateral habenula, magnocellular preoptic nucleus, lateral hypothalamus, GABAergic neurons, dopaminergic neurons, appetitive motivation
MeSH terms: Animals, Efferent Pathways, Female, Phytohemagglutinins, Prosencephalon, Rats, Wistar, Ventral Tegmental Area, Rats

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Efferent connections of the rostral linear nucleus of the ventral tegmental area in the rat

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