Skip to main content

Advertisement

Log in

Organization of brain somatomotor-sympathetic circuits

  • Review
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Numerous physiological and emotionally motivated behaviors require concomitant activation of somatomotor and sympathetic efferents. Likewise, adaptive and maladaptive responses to stress are often characterized by simultaneous recruitment of these efferent systems. This review describes recent literature that outlines the organization of somatomotor-sympathetic circuitry in the rat. These circuits were delineated by employing recombinant pseudorabies (PRV) viral vectors as retrograde trans-synaptic tract tracers. In these studies PRV-152, a strain that expresses enhanced green fluorescent protein, was injected into sympathectomized hindlimb muscle, while PRV–BaBlu, which expresses β-galactosidase, was injected into the adrenal gland in the same animals. Immunofluorescent methods were then used to determine the presence of putative dual-function neurons that were infected with both viral strains. These somatomotor-sympathetic neurons (SMSNs) were detected in a number of brain regions. However, the most prominent nodes in this circuitry included the paraventricular, dorsomedial, and lateral nuclei of the hypothalamus, ventrolateral periaqueductal grey and ventromedial medulla. Phenotypic studies revealed subsets of SMSNs to be capable of synthesizing serotonin, or to contain neuroactive peptides vasopressin, oxytocin, orexins, or melanin-concentrating hormone. Based on these data and the results of studies employing monosynaptic tracers a central somatomotor-sympathetic circuit is proposed. This circuitry is likely recruited in diverse situations, including stress responses, cold defense, exercise and sleep. Furthermore, activation of specific classes of SMSNs likely shapes distinct stress-coping strategies. Dysregulation in the organization and function of this circuit may also contribute to the expression of physical symptoms of affective disorders, such as major depression, anxiety and panic.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Allen GV, Cechetto DF (1992) Functional and anatomical organization of cardiovascular pressor and depressor sites in the lateral hypothalamic area: I. Descending projections. J Comp Neurol 315:313–332

    PubMed  CAS  Google Scholar 

  • Allen GV, Cechetto DF (1994) Serotoninergic and nonserotoninergic neurons in the medullary raphe system have axon collateral projections to autonomic and somatic cell groups in the medulla and spinal cord. J Comp Neurol 350:357–366

    PubMed  CAS  Google Scholar 

  • Arborelius L, Owens MJ, Plotsky PM, Nemeroff CB (1999) The role of corticotropin-releasing factor in depression and anxiety disorders. J Endocrinol 160:1–12

    PubMed  CAS  Google Scholar 

  • Argyropoulos SV, Hood SD, Adrover M, Bell CJ, Rich AS, Nash JR, Rich NC, Witchel HJ, Nutt DJ (2004) Tryptophan depletion reverses the therapeutic effect of selective serotonin reuptake inhibitors in social anxiety disorder. Biol Psychiatry 56:503–509

    PubMed  CAS  Google Scholar 

  • Ariyo AA, Haan M, Tangen CM, Rutledge JC, Cushman M, Dobs A, Furberg CD (2000) Depressive symptoms and risks of coronary heart disease and mortality in elderly Americans. Cardiovascular Health Study Collaborative Research Group. Circulation 102:1773–1779

    PubMed  CAS  Google Scholar 

  • Aston-Jones G, Shipley MT, Grzanna R (1995) The locus coeruleus, A5 and A7 noradrenergic cell groups. In: Paxinos G (ed) The rat nervous system. Academic Press, San Diego, pp 183–213

    Google Scholar 

  • Bandler R, Price JL, Keay KA (2000) Brain mediation of active and passive emotional coping. Progress Brain Res 122:333–349

    CAS  Google Scholar 

  • Beitz AJ, Shepard RD, Wells WE (1983) The periaqueductal gray-raphe magnus projection contains somatostatin, neurotensin and serotonin but not cholecystokinin. Brain Res 261:132–137

    PubMed  CAS  Google Scholar 

  • Benarroch EB (1993) The central autonomic network: functional organization, dysfunction, and perspective. Mayo Clinic Proc 68:988–1001

    CAS  Google Scholar 

  • Billig I, Foris JM, Card JP, Yates BJ (1999) Transneuronal tracing of neural pathways controlling an abdominal muscle, rectus, abdominis in the ferret. Brain Res 820:31–44

    PubMed  CAS  Google Scholar 

  • Billig I, Foris JM, Enquist LW, Card JP, Yates BJ (2000) Definition of neuronal circuitry controlling the activity of phrenic and abdominal motoneurons in the ferret using recombinant strains of pseudorabies virus. J Neurosci 20:7446–7454

    PubMed  CAS  Google Scholar 

  • Billig I, Hartge K, Card JP, Yates BJ (2001) Transneuronal tracing of neural pathways controlling abdominal musculature in the ferret. Brain Res 912:24–32

    PubMed  CAS  Google Scholar 

  • Bittencourt JC, Presse F, Arias C, Peto C, Vaughan J, Nahon JL, Vale W, Sawchenko PE (1992) The melanin-concentrating hormone system of the rat brain: an immuno- and hybridization histochemical characterization. J Comp Neurol 319:218–245

    PubMed  CAS  Google Scholar 

  • Cameron OG, Huang GC, Nichols T, Koeppe RA, Minoshima S, Rose D, Frey KA (2007) Reduced gamma-aminobutyric acid(A)-benzodiazepine binding sites in insular cortex of individuals with panic disorder. Arch Gen Psychiatry 64:793–800

    PubMed  CAS  Google Scholar 

  • Cannon WB (1963) The wisdom of the body. W. W. Norton, New York

    Google Scholar 

  • Cano G, Card JP, Sved AF (2004) Dual viral transneuronal tracing of central autonomic circuits involved in the innervation of the two kidneys in rat. J Comp Neurol 471:462–481

    PubMed  Google Scholar 

  • Card JP (2001) Pseudorabies virus neuroinvasiveness: a window into the functional organization of the brain. Adv Virus Res 56:39–71

    PubMed  CAS  Google Scholar 

  • Card JP, Enquist LW (1999) Transneuronal circuit analysis with pseudorabies virus. In: Neuroanatomical methods, vol Suppl 9. Wiley, New York, pp 1.5.1–1.5.28

  • Card JP, Rinaman L, Lynn RB, Lee BH, Meade RP, Miselis RR, Enquist LW (1993) Pseudorabies virus infection of the rat central nervous system: ultrastructural characterization of viral replication, transport, and pathogenesis. J Neurosci 13:2515–2539

    PubMed  CAS  Google Scholar 

  • Card JP, Levitt P, Gluhovsky M, Rinaman L (2005) Early experience modifies the postnatal assembly of autonomic emotional motor circuits in rats. J Neurosci 25:9102–9111

    PubMed  CAS  Google Scholar 

  • Carrive P, Bandler R (1991) Viscerotopic organization of neurons subserving hypotensive reactions within the midbrain periaqueductal grey: a correlative functional and anatomical study. Brain Res 541:206–215

    PubMed  CAS  Google Scholar 

  • Caspi A, Sugden K, Moffitt TE, Taylor A, Craig IW, Harrington H, McClay J, Mill J, Martin J, Braithwaite A, Poulton R (2003) Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 301:386–389

    PubMed  CAS  Google Scholar 

  • Depaulis A, Keay KA, Bandler R (1994) Quiescence and hyporeactivity evoked by activation of cell bodies in the ventrolateral midbrain periaqueductal gray of the rat. Exp Brain Res 99:75–83

    PubMed  CAS  Google Scholar 

  • DiMicco JA, Samuels BC, Zaretskaia MV, Zaretsky DV (2002) The dorsomedial hypothalamus and the response to stress: part renaissance, part revolution. Pharmacol Biochem Behav 71:469–480

    PubMed  CAS  Google Scholar 

  • Elias CF, Sita LV, Zambon BK, Oliveira ER, Vasconcelos LA, Bittencourt JC (2008) Melanin-concentrating hormone projections to areas involved in somatomotor responses. J Chem Neuroanat 35:188–201

    PubMed  CAS  Google Scholar 

  • Famularo R, Kinscherff R, Fenton T (1992) Psychiatric diagnoses of maltreated children: preliminary findings. J Am Acad Child Adolesc Psychiatry 31:863–867

    PubMed  CAS  Google Scholar 

  • Fava M, Kendler KS (2000) Major depressive disorder. Neuron 28:335–341

    PubMed  CAS  Google Scholar 

  • Flint AJ, Black SE, Campbell-Taylor I, Gailey GF, Levinton C (1993) Abnormal speech articulation, psychomotor retardation, and subcortical dysfunction in major depression. J Psychiatr Res 27:309–319

    PubMed  CAS  Google Scholar 

  • Ford DE, Mead LA, Chang PP, Cooper-Patrick L, Wang NY, Klag MJ (1998) Depression is a risk factor for coronary artery disease in men: the precursors study. Arch Intern Med 158:1422–1426

    PubMed  CAS  Google Scholar 

  • Futuro-Neto HA, Coote JH (1982a) Changes in sympathetic activity to heart and blood vessels during desynchronized sleep. Brain Res 252:259–268

    PubMed  CAS  Google Scholar 

  • Futuro-Neto HA, Coote JH (1982b) Desynchronized sleep-like pattern of sympathetic activity elicited by electrical stimulation of sites in the brainstem. Brain Res 252:269–276

    PubMed  CAS  Google Scholar 

  • Gao XB, van den Pol AN (2001) Melanin concentrating hormone depresses synaptic activity of glutamate and GABA neurons from rat lateral hypothalamus. J Physiol 533:237–252

    PubMed  CAS  Google Scholar 

  • Glassman AH (2007) Depression and cardiovascular comorbidity. Dialogues Clin Neurosci 9:9–17

    PubMed  Google Scholar 

  • Gliatto MF (2000) Generalized anxiety disorder. Am Fam Physician 62:1591–1600, 1602

    Google Scholar 

  • Hallbeck M, Blomqvist A (1999) Spinal cord-projecting vasopressinergic neurons in the rat paraventricular hypothalamus. J Comp Neurol 411:201–211

    PubMed  CAS  Google Scholar 

  • Hallbeck M, Larhammar D, Blomqvist A (2001) Neuropeptide expression in rat paraventricular hypothalamic neurons that project to the spinal cord. J Comp Neurol 433:222–238

    PubMed  CAS  Google Scholar 

  • Hardy P, Jouvent R, Widlocher D (1984) Speech pause time and the retardation rating scale for depression (ERD). Towards a reciprocal validation. J Affect Disord 6:123–127

    PubMed  CAS  Google Scholar 

  • Haring JH, Davis JN (1983) Acetylcholinesterase neurons in the lateral hypothalamus project to the spinal cord. Brain Res 268:275–283

    PubMed  CAS  Google Scholar 

  • Harmon AC, Huhman KL, Moore TO, Albers HE (2002) Oxytocin inhibits aggression in female Syrian hamsters. J Neuroendocrinol 14:963–969

    PubMed  CAS  Google Scholar 

  • Herman JP, Cullinan WE (1997) Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci 20:78–84

    PubMed  CAS  Google Scholar 

  • Hermann DM, Luppi PH, Peyron C, Hinckel P, Jouvet M (1997) Afferent projections to the rat nuclei raphe magnus, raphe pallidus and reticularis gigantocellularis pars alpha demonstrated by iontophoretic application of choleratoxin (subunit b). J Chem Neuroanat 13:1–21

    PubMed  CAS  Google Scholar 

  • Hilton SM (1982) The defence-arousal system and its relevance for circulatory and respiratory control. J Exp Biol 100:159–174

    PubMed  CAS  Google Scholar 

  • Holstege G (1995) The basic, somatic, and emotional components of the motor system in mammals. In: Paxinos G (ed) The rat nervous system. Academic Press, San Diego

    Google Scholar 

  • Holstege JC (1996) The ventro-medial medullar projections to spinal motoneurons: ultrastructure, transmitters and functional aspects. In: Holstege G, Bandler R, Saper CB (eds) Progress in brain research, vol 107, pp 159–181

  • Holstege JC, Kuypers HG (1987) Brainstem projections to spinal motoneurons: an update. Neuroscience 23:809–821

    PubMed  CAS  Google Scholar 

  • Horiuchi J, McAllen RM, Allen AM, Killinger S, Fontes MA, Dampney RA (2004) Descending vasomotor pathways from the dorsomedial hypothalamic nucleus: role of medullary raphe and RVLM. Am J Physiol Regul Integr Comp Physiol 287:R824–R832

    PubMed  CAS  Google Scholar 

  • Hosoya Y (1980) The distribution of spinal projection neurons in the hypothalamus of the rat, studied with the HRP method. Exp Brain Res 40:79–87

    PubMed  CAS  Google Scholar 

  • Hosoya Y (1985) Hypothalamic projections to the ventral medulla oblongata in the rat, with special reference to the nucleus raphe pallidus: a study using autoradiographic and HRP techniques. Brain Res 344:338–350

    PubMed  CAS  Google Scholar 

  • Hurley KM, Herbert H, Moga MM, Saper CB (1991) Efferent projections of the infralimbic cortex of the rat. J Comp Neurol 308:249–276

    PubMed  CAS  Google Scholar 

  • Jacobs BL, Fornal CA (1997) Serotonin and motor activity. Curr Opin Neurobiol 7:820–825

    PubMed  CAS  Google Scholar 

  • Jacobs BL, Martin-Cora FJ, Fornal CA (2002) Activity of medullary serotonergic neurons in freely moving animals. Brain Res Brain Res Rev 40:45–52

    PubMed  CAS  Google Scholar 

  • Jänig W (1988) Pre- and postganglionic vasoconstrictor neurons: differentiation, types, and discharge properties. Ann Rev Physiol 50:525–539

    Google Scholar 

  • Jansen ASP, Farwell DG, Loewy AD (1993) Specificity of pseudorabies virus as a retrograde marker of sympathetic preganglionic neurons: implications for transneuronal labeling studies. Brain Res 617:103–112

    PubMed  CAS  Google Scholar 

  • Jansen AS, Nguyen XV, Karpitskiy V, Mettenleiter TC, Loewy AD (1995) Central command neurons of the sympathetic nervous system: basis of the fight-or-flight response. Science 270:644–646

    PubMed  CAS  Google Scholar 

  • Jiang W, Kuchibhatla M, Cuffe MS, Christopher EJ, Alexander JD, Clary GL, Blazing MA, Gaulden LH, Califf RM, Krishnan RR, O’Connor CM (2004) Prognostic value of anxiety and depression in patients with chronic heart failure. Circulation 110:3452–3456

    PubMed  CAS  Google Scholar 

  • Johnson AK, Grippo AJ (2006) Sadness and broken hearts: neurohumoral mechanisms and co-morbidity of ischemic heart disease and psychological depression. J Physiol Pharmacol 57 Suppl 11:5–29

    Google Scholar 

  • Johnson PL, Truitt W, Fitz S, Dietrich A, Lowry CA, Shekhar A (2007) Disruption of GABAergic tone in the dorsomedial hypothalamus attenuates responses in a subset of serotonergic neurons in the dorsal raphe nucleus following lactate-induced panic. In: Annual society for neuroscience meeting, San Diego

  • Jones SL, Light AR (1990) Termination patterns of serotoninergic medullary raphespinal fibers in the rat lumbar spinal cord: an anterograde immunohistochemical study. J Comp Neurol 297:267–282

    PubMed  CAS  Google Scholar 

  • Jones SL, Light AR (1992) Serotoninergic medullary raphespinal projection to the lumbar spinal cord in the rat: a retrograde immunohistochemical study. J Comp Neurol 322:599–610

    PubMed  CAS  Google Scholar 

  • Jordan D (1990) Autonomic changes in affective behavior. In: Loewy AD, Spyer KM (eds) Central regulation of autonomic functions. Oxford University Press, New York, pp 349–366

    Google Scholar 

  • Kandel ER, Schwartz JH, Jessell TM (2000) Principles of neural science. McGraw-Hill, New York

    Google Scholar 

  • Kasckow JW, Baker D, Geracioti TD Jr (2001) Corticotropin-releasing hormone in depression and post-traumatic stress disorder. Peptides 22:845–851

    PubMed  CAS  Google Scholar 

  • Kaufman J, Plotsky PM, Nemeroff CB, Charney DS (2000) Effects of early adverse experiences on brain structure and function: clinical implications. Biol Psychiatry 48:778–790

    PubMed  CAS  Google Scholar 

  • Kayaba Y, Nakamura A, Kasuya Y, Ohuchi T, Yanagisawa M, Komuro I, Fukuda Y, Kuwaki T (2003) Attenuated defense response and low basal blood pressure in orexin knockout mice. Am J Physiol Regul Integr Comp Physiol 285:R581–R593

    PubMed  Google Scholar 

  • Kerman IA, Akil H, Watson SJ (2006a) Rostral elements of sympatho-motor circuitry: a virally-mediated transsynaptic tracing study. J Neurosci 26:3423–3433

    PubMed  CAS  Google Scholar 

  • Kerman IA, Enquist LW, Watson SJ, Yates BJ (2003) Brainstem substrates of sympatho-motor circuitry identified using trans-synaptic tracing with pseudorabies virus recombinants. J Neurosci 23:4657–4666

    PubMed  CAS  Google Scholar 

  • Kerman IA, Shabrang C, Taylor L, Akil H, Watson SJ (2006b) Relationship of presympathetic-premotor neurons to the serotonergic transmitter system in the rat brainstem. J Comp Neurol 499:882–896

    PubMed  CAS  Google Scholar 

  • Kerman IA, Bernard R, Rosenthal D, Beals J, Akil H, Watson SJ (2007) Distinct populations of presympathetic-premotor neurons express orexin or melanin-concentrating hormone in the rat lateral hypothalamus. J Comp Neurol 505:586–601

    PubMed  Google Scholar 

  • Kim JS, Enquist LW, Card JP (1999) Circuit-specific coinfection of neurons in the rat central nervous system with two pseudorabies virus recombinants. J Virol 73:9521–9531

    PubMed  CAS  Google Scholar 

  • Kohler C, Haglund L, Swanson LW (1984) A diffuse alpha MSH-immunoreactive projection to the hippocampus and spinal cord from individual neurons in the lateral hypothalamic area and zona incerta. J Comp Neurol 223:501–514

    PubMed  CAS  Google Scholar 

  • Kollack-Walker S, Watson SJ, Akil H (1997) Social stress in hamsters: defeat activates specific neurocircuits within the brain. J Neurosci 17:8842–8855

    PubMed  CAS  Google Scholar 

  • Kreier F, Kap YS, Mettenleiter TC, van Heijningen C, van der Vliet J, Kalsbeek A, Sauerwein HP, Fliers E, Romijn JA, Buijs RM (2006) Tracing from fat tissue, liver, and pancreas:a neuroanatomical framework for the role of the brain in type 2 diabetes. Endocrinology 147:1140–1147

    PubMed  CAS  Google Scholar 

  • Kunos G, Varga K (1995) The tachycardia associated with the defense reaction involves activation of both GABAA and GABAB receptors in the nucleus tractus solitarii. Clin Exp Hypertens 17:91–100

    PubMed  CAS  Google Scholar 

  • Ladd CO, Huot RL, Thrivikraman KV, Nemeroff CB, Meaney MJ, Plotsky PM (2000) Long-term behavioral and neuroendocrine adaptations to adverse early experience. Prog Brain Res 122:81–103

    PubMed  CAS  Google Scholar 

  • Langley JN (1921) The autonomic nervous system. W. Heffer, Cambridge

    Google Scholar 

  • Lee JH, Kim HJ, Kim JG, Ryu V, Kim BT, Kang DW, Jahng JW (2007) Depressive behaviors and decreased expression of serotonin reuptake transporter in rats that experienced neonatal maternal separation. Neurosci Res 58:32–39

    PubMed  CAS  Google Scholar 

  • Lemke MR, Wendorff T, Mieth B, Buhl K, Linnemann M (2000) Spatiotemporal gait patterns during over ground locomotion in major depression compared with healthy controls. J Psychiatr Res 34:277–283

    PubMed  CAS  Google Scholar 

  • Lesperance F, Frasure-Smith N, Talajic M, Bourassa MG (2002) Five-year risk of cardiac mortality in relation to initial severity and one-year changes in depression symptoms after myocardial infarction. Circulation 105:1049–1053

    PubMed  Google Scholar 

  • Lewis DI, Sermasi E, Coote JH (1993) Excitatory and indirect inhibitory actions of 5-hydroxytryptamine on sympathetic preganglionic neurones in the neonate rat spinal cord in vitro. Brain Res 610:267–275

    PubMed  CAS  Google Scholar 

  • Liebowitz MR, Fyer AJ, Gorman JM, Dillon D, Appleby IL, Levy G, Anderson S, Levitt M, Palij M, Davies SO et al. (1984) Lactate provocation of panic attacks. I. Clinical and behavioral findings. Arch Gen Psychiatry 41:764–770

    PubMed  CAS  Google Scholar 

  • Liebowitz MR, Gorman JM, Fyer AJ, Levitt M, Dillon D, Levy G, Appleby IL, Anderson S, Palij M, Davies SO et al (1985) Lactate provocation of panic attacks. II. Biochemical and physiological findings. Arch Gen Psychiatry 42:709–719

    PubMed  CAS  Google Scholar 

  • Loewy AD (1990) Central autonomic pathways. In: Loewy AD, Spyer KM (eds) Central regulation of autonomic functions. Oxford University Press, New York, pp 89–103

    Google Scholar 

  • Lovick TA (1992) Inhibitory modulation of the cardiovascular defence response by the ventrolateral periaqueductal grey matter in rats. Exp Brain Res 89:133–139

    PubMed  CAS  Google Scholar 

  • Madden CJ, Morrison SF (2006) Serotonin potentiates sympathetic responses evoked by spinal NMDA. J Physiol 577:525–537

    PubMed  CAS  Google Scholar 

  • Mancia G, Zanchetti A (1981) Hypothalamic control of autonomic functions. In: Morgane PJ, Panksepp J (eds) Behavioral studies of the hypothalamus. Marcel Dekker, New York, pp 147–202

    Google Scholar 

  • Marsh DJ, Weingarth DT, Novi DE, Chen HY, Trumbauer ME, Chen AS, Guan XM, Jiang MM, Feng Y, Camacho RE, Shen Z, Frazier EG, Yu H, Metzger JM, Kuca SJ, Shearman LP, Gopal-Truter S, MacNeil DJ, Strack AM, MacIntyre DE, Van der Ploeg LH, Qian S (2002) Melanin-concentrating hormone 1 receptor-deficient mice are lean, hyperactive, and hyperphagic and have altered metabolism. Proc Natl Acad Sci USA 99:3240–3245

    PubMed  CAS  Google Scholar 

  • Marson L, Foley KA (2004) Identification of neural pathways involved in genital reflexes in the female: a combined anterograde and retrograde tracing study. Neuroscience 127:723–736

    PubMed  CAS  Google Scholar 

  • Martin GF, Humbertson AO, Laxson C, Panneton WM (1979) Evidence for direct bulbospinal projections to laminae IX, X and the intermediolateral cell column. Studies using axonal transport techniques in the North American opossum. Brain Res 170:165–171

    PubMed  CAS  Google Scholar 

  • Martin GF, Vertes RP, Waltzer R (1985) Spinal projections of the gigantocellular reticular formation in the rat. Evidence for projections from different areas to laminae I and II and lamina IX. Exp Brain Res 58:154–162

    PubMed  CAS  Google Scholar 

  • Mason P (2001) Contributions of the medullary raphe and ventromedial reticular region to pain modulation and other homeostatic functions. Ann Rev Neurosci 24:737–777

    PubMed  CAS  Google Scholar 

  • Mason P (2005) Ventromedial medulla: pain modulation and beyond. J Comp Neurol 493:2–8

    PubMed  Google Scholar 

  • McAllen RM (2007) The cold path to BAT. Am J Physiol Regul Integr Comp Physiol 292:R124–R126

    PubMed  CAS  Google Scholar 

  • McCormick CM, Merrick A, Secen J, Helmreich DL (2007) Social instability in adolescence alters the central and peripheral hypothalamic–pituitary–adrenal responses to a repeated homotypic stressor in male and female rats. J Neuroendocrinol 19:116–126

    PubMed  CAS  Google Scholar 

  • McDowall LM, Horiuchi J, Dampney RA (2007) Effects of disinhibition of neurons in the dorsomedial hypothalamus on central respiratory drive. Am J Physiol Regul Integr Comp Physiol 293:R1728–R1735

    PubMed  CAS  Google Scholar 

  • Messina MM, Overton JM (2007) Cardiovascular effects of melanin-concentrating hormone. Regul Pept 139:23–30

    PubMed  CAS  Google Scholar 

  • Morgan MM, Carrive P (2001) Activation of the ventrolateral periaqueductal gray reduces locomotion but not mean arterial pressure in awake, freely moving rats. Neuroscience 102:905–910

    PubMed  CAS  Google Scholar 

  • Morgan MM, Whitney PK, Gold MS (1998) Immobility and flight associated with antinociception produced by activation of the ventral and lateral/dorsal regions of the rat periaqueductal gray. Brain Res 804:159–166

    PubMed  CAS  Google Scholar 

  • Morrison SF (2004) Central pathways controlling brown adipose tissue thermogenesis. News Physiol Sci 19:67–74

    PubMed  Google Scholar 

  • Mouton LJ, Holstege G (1994) The periaqueductal gray in the cat projects to lamina VIII and the medial part of lamina VII throughout the length of the spinal cord. Exp Brain Res 101:253–264

    PubMed  CAS  Google Scholar 

  • Murgatroyd C, Wigger A, Frank E, Singewald N, Bunck M, Holsboer F, Landgraf R, Spengler D (2004) Impaired repression at a vasopressin promoter polymorphism underlies overexpression of vasopressin in a rat model of trait anxiety. J Neurosci 24:7762–7770

    PubMed  CAS  Google Scholar 

  • Nason MW Jr, Mason P (2004) Modulation of sympathetic and somatomotor function by the ventromedial medulla. J Neurophysiol 92:510–522

    PubMed  Google Scholar 

  • Nemeroff CB (1996) The corticotropin-releasing factor (CRF) hypothesis of depression:new findings and new directions. Mol Psychiatry 1:336–342

    PubMed  CAS  Google Scholar 

  • Nestler EJ, Barrot M, DiLeone RJ, Eisch AJ, Gold SJ, Monteggia LM (2002) Neurobiology of depression. Neuron 34:13–25

    PubMed  CAS  Google Scholar 

  • Nijsen MJ, Croiset G, Stam R, Bruijnzeel A, Diamant M, de Wied D, Wiegant VM (2000) The role of the CRH type 1 receptor in autonomic responses to corticotropin- releasing hormone in the rat. Neuropsychopharmacology 22:388–399

    PubMed  CAS  Google Scholar 

  • Pajolla GP, de Aguiar Correa FM (2004) Cardiovascular responses to the injection of L-glutamate in the lateral hypothalamus of unanesthetized or anesthetized rats. Auton Neurosci 116:19–29

    PubMed  CAS  Google Scholar 

  • Patel P, Pontrello C, Burke S (2004) Robust and tissue-specific expression of TPH2 versus TPH1 in rat raphe and pineal gland. Biol Psychiatry 55:428–433

    PubMed  CAS  Google Scholar 

  • Plotsky PM, Meaney MJ (1993) Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Brain Res Mol Brain Res 18:195–200

    PubMed  CAS  Google Scholar 

  • Porter JP, Brody MJ (1986) A comparison of the hemodynamic effects produced by electrical stimulation of subnuclei of the paraventricular nucleus. Brain Res 375:20–29

    PubMed  CAS  Google Scholar 

  • Ragnauth AK, Devidze N, Moy V, Finley K, Goodwillie A, Kow LM, Muglia LJ, Pfaff DW (2005) Female oxytocin gene-knockout mice, in a semi-natural environment, display exaggerated aggressive behavior. Genes Brain Behav 4:229–239

    PubMed  CAS  Google Scholar 

  • Rinaman L, Card JP, Enquist LW (1993) Spatiotemporal responses of astrocytes, ramified microglia, and brain macrophages to central neuronal infection with pseudorabies virus. J Neurosci 13:685–702

    PubMed  CAS  Google Scholar 

  • Roth WT (2005) Physiological markers for anxiety: panic disorder and phobias. Int J Psychophysiol 58:190–198

    PubMed  Google Scholar 

  • Sabbe B, Hulstijn W, van Hoof J, Tuynman-Qua HG, Zitman F (1999) Retardation in depression: assessment by means of simple motor tasks. J Affect Disord 55:39–44

    PubMed  CAS  Google Scholar 

  • Sabbe B, Hulstijn W, Van Hoof J, Zitman F (1996) Fine motor retardation and depression. J Psychiatr Res 30:295–306

    PubMed  CAS  Google Scholar 

  • Sakurai T, Amemiya A, Ishii M, Matsuzaki I, Chemelli RM, Tanaka H, Williams SC, Richardson JA, Kozlowski GP, Wilson S, Arch JR, Buckingham RE, Haynes AC, Carr SA, Annan RS, McNulty DE, Liu WS, Terrett JA, Elshourbagy NA, Bergsma DJ, Yanagisawa M (1998) Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92:573–585

    PubMed  CAS  Google Scholar 

  • Saper CB, Loewy AD, Swanson LW, Cowan WM (1976) Direct hypothalamo-autonomic connections. Brain Res 117:305–312

    PubMed  CAS  Google Scholar 

  • Saper CB, Swanson LW, Cowan WM (1979) An autoradiographic study of the efferent connections of the lateral hypothalamic area in the rat. J Comp Neurol 183:689–706

    PubMed  CAS  Google Scholar 

  • Sawchenko PE (1987) Evidence for differential regulation of corticotropin-releasing factor and vasopressin immunoreactivities in parvocellular neurosecretory and autonomic-related projections of the paraventricular nucleus. Brain Res 437:253–263

    PubMed  CAS  Google Scholar 

  • Sawchenko PE, Brown ER, Chan RK, Ericsson A, Li HY, Roland BL, Kovacs KJ (1996) The paraventricular nucleus of the hypothalamus and the functional neuroanatomy of visceromotor responses to stress. Prog Brain Res 107:201–222

    PubMed  CAS  Google Scholar 

  • Shekhar A, Keim SR, Simon JR, McBride WJ (1996) Dorsomedial hypothalamic GABA dysfunction produces physiological arousal following sodium lactate infusions. Pharmacol Biochem Behav 55:249–256

    PubMed  CAS  Google Scholar 

  • Shiosaka S, Kawai Y, Shibasaki T, Tohyama M (1985) The descending alpha-MSHergic (alpha-melanocyte-stimulating hormone-ergic) projections from the zona incerta and lateral hypothalamic area to the inferior colliculus and spinal cord in the rat. Brain Res 338:371–375

    PubMed  CAS  Google Scholar 

  • Shumake J, Edwards E, Gonzalez-Lima F (2001) Hypermetabolism of paraventricular hypothalamus in the congenitally helpless rat. Neurosci Lett 311:45–48

    PubMed  CAS  Google Scholar 

  • Skagerberg G, Björklund A (1985) Topographic principles in the spinal projections of serotonergic and non-serotonergic brainstem neurons in the rat. Neuroscience 15:445–480

    PubMed  CAS  Google Scholar 

  • Sloman L, Berridge M, Homatidis S, Hunter D, Duck T (1982) Gait patterns of depressed patients and normal subjects. Am J Psychiatry 139:94–97

    PubMed  CAS  Google Scholar 

  • Smith BN, Banfield BW, Smeraski CA, Wilcox CL, Dudek FE, Enquist LW, Pickard GE (2000) Pseudorabies virus expressing enhanced green fluorescent protein: a tool for in vitro electrophysiological analysis of transsynaptically labeled neurons in identified central nervous system circuits. Proc Natl Acad Sci USA 97:9264–9269

    PubMed  CAS  Google Scholar 

  • Sobin C, Sackeim HA (1997) Psychomotor symptoms of depression. Am J Psychiatry 154:4–17

    PubMed  CAS  Google Scholar 

  • Standish A, Enquist LW, Miselis RR, Schwaber JS (1995) Dendritic morphology of cardiac related medullary neurons defined by circuit-specific infection by a recombinant pseudorabies virus expressing beta-galactosidase. J Neurovirol 1:359–368

    PubMed  CAS  Google Scholar 

  • Stocker SD, Cunningham JT, Toney GM (2004) Water deprivation increases Fos immunoreactivity in PVN autonomic neurons with projections to the spinal cord and rostral ventrolateral medulla. Am J Physiol Regul Integr Comp Physiol 287:R1172–1183

    PubMed  CAS  Google Scholar 

  • Strack AM, Sawyer WB, Hughes JH, Platt KB, Loewy AD (1989a) A general pattern of CNS innervation of the sympathetic outflow demonstrated by transneuronal pseudorabies viral infections. Brain Res 491:156–162

    PubMed  CAS  Google Scholar 

  • Strack AM, Sawyer WB, Platt KB, Loewy AD (1989b) CNS cell groups regulating the sympathetic outflow to adrenal gland as revealed by transneuronal cell body labeling with pseudorabies virus. Brain Res 491:274–296

    PubMed  CAS  Google Scholar 

  • Sutcliffe JG, de Lecea L (2000) The hypocretins: excitatory neuromodulatory peptides for multiple homeostatic systems, including sleep and feeding. J Neurosci Res 62:161–168

    PubMed  CAS  Google Scholar 

  • Sved AF, Cano G, Card JP (2001) Neuroanatomical specificity of the circuits controlling sympathetic outflow to different targets. Clin Exp Pharmacol Physiol 28:115–119

    PubMed  CAS  Google Scholar 

  • Swanson LW, Kuypers HG (1980) The paraventricular nucleus of the hypothalamus: cytoarchitectonic subdivisions and organization of projections to the pituitary, dorsal vagal complex, and spinal cord as demonstrated by retrograde fluorescence double-labeling methods. J Comp Neurol 194:555–570

    PubMed  CAS  Google Scholar 

  • Swanson LW, Sanchez-Watts G, Watts AG (2005) Comparison of melanin-concentrating hormone and hypocretin/orexin mRNA expression patterns in a new parceling scheme of the lateral hypothalamic zone. Neurosci Lett 387:80–84

    PubMed  CAS  Google Scholar 

  • Tanaka M, McAllen RM (2008) Functional topography of the dorsomedial hypothalamus. Am J Physiol Regul Integr Comp Physiol 294:R477–R486

    PubMed  CAS  Google Scholar 

  • Tanaka M, Owens NC, Nagashima K, Kanosue K, McAllen RM (2006) Reflex activation of rat fusimotor neurons by body surface cooling, and its dependence on the medullary raphe. J Physiol 572:569–583

    PubMed  CAS  Google Scholar 

  • ter Horst GJ, Luiten PG (1986) The projections of the dorsomedial hypothalamic nucleus in the rat. Brain Res Bull 16:231–248

    PubMed  CAS  Google Scholar 

  • Thompson RH, Canteras NS, Swanson LW (1996) Organization of projections from the dorsomedial nucleus of the hypothalamus: a PHA-L study in the rat. J Comp Neurol 376:143–173

    PubMed  CAS  Google Scholar 

  • Truitt WA, Johnson PL, Sanghani S, Engleman E, Kelley P, Shekhar A (2007) Silencing of the preproorexin gene in the hypothalamus attenuates lactate-induced panic-like responses in the rat. In: Annual Society for Neuroscience Meeting, San Diego

  • Van Bockstaele EJ, Aston-Jones G, Pieribone VA, Ennis M, Shipley MT (1991) Subregions of the periaqueductal gray topographically innervate the rostral ventral medulla in the rat. J Comp Neurol 309:305–327

    PubMed  Google Scholar 

  • Verberne AJ, Lam W, Owens NC, Sartor D (1997) Supramedullary modulation of sympathetic vasomotor function. Clin Exp Pharmacol Physiol 24:748–754

    PubMed  CAS  Google Scholar 

  • Viau V, Sawchenko PE (2002) Hypophysiotropic neurons of the paraventricular nucleus respond in spatially, temporally, and phenotypically differentiated manners to acute vs. repeated restraint stress: Rapid publication. J Comp Neurol 445:293–307

    PubMed  Google Scholar 

  • Waldrop TG, Eldridge FL, Iwamoto GA, Mitchell JH (1996) Central neural control of respiration and circulation during exercise. In: Rowell LB, Shepherd JT (eds) Handbook of physiology. Section 12: Exercise: regulation and integration of multiple systems. Oxford University Press, New York, pp 333–380

  • Walther DJ, Peter JU, Bashammakh S, Hortnagl H, Voits M, Fink H, Bader M (2003) Synthesis of serotonin by a second tryptophan hydroxylase isoform. Science 299:76

    PubMed  CAS  Google Scholar 

  • White SR, Fung SJ, Jackson DA, Imel KM (1996) Serotonin, norepinephrine and associated neuropeptides: effects on somatic motoneuron excitability. Prog Brain Res 107:183–199

    Article  PubMed  CAS  Google Scholar 

  • Yasui Y, Breder CD, Saper CB, Cechetto DF (1991) Autonomic responses and efferent pathways from the insular cortex in the rat. J Comp Neurol 303:355–374

    PubMed  CAS  Google Scholar 

  • Yates WR, Mitchell J, Rush AJ, Trivedi MH, Wisniewski SR, Warden D, Hauger RB, Fava M, Gaynes BN, Husain MM, Bryan C (2004) Clinical features of depressed outpatients with and without co-occurring general medical conditions in STAR*D. Gen Hosp Psychiatry 26:421–429

    PubMed  Google Scholar 

  • Yates WR, Mitchell J, John Rush A, Trivedi M, Wisniewski SR, Warden D, Bryan C, Fava M, Husain MM, Gaynes BN (2007) Clinical features of depression in outpatients with and without co-occurring general medical conditions in STAR*D: confirmatory analysis. Prim Care Companion J Clin Psychiatry 9:7–15

    PubMed  Google Scholar 

  • Zaretsky DV, Zaretskaia MV, Samuels BC, Cluxton LK, DiMicco JA (2003) Microinjection of muscimol into raphe pallidus suppresses tachycardia associated with air stress in conscious rats. J Physiol 546:243–250

    PubMed  CAS  Google Scholar 

  • Zemlan FP, Behbehani MM, Beckstead RM (1984) Ascending and descending projections from nucleus reticularis magnocellularis and nucleus reticularis gigantocellularis: an autoradiographic and horseradish peroxidase study in the rat. Brain Res 292:207–220

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The author is grateful to Drs. Sarah M. Clinton and Stanley J. Watson for critical reading of an earlier version of the manuscript. IAK is supported by NARSAD Young Investigator Award and the University of Michigan Comprehensive Depression Center Innovation Fund Grant Program. Throughout the course of these studies PRV strains were provided by L. W. Enquist, Princeton University as a service of the National Center for Experimental Neuroanatomy with Neurotropic Viruses: NCRR P40 RRO118604.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ilan A. Kerman.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kerman, I.A. Organization of brain somatomotor-sympathetic circuits. Exp Brain Res 187, 1–16 (2008). https://doi.org/10.1007/s00221-008-1337-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-008-1337-5

Keywords

Navigation