Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1980 Jan;298:53–70. doi: 10.1113/jphysiol.1980.sp013066

Electrophysiological analysis of pathways connecting the medial preoptic area with the mesencephalic central grey matter in rats.

N K MacLeod, M L Mayer
PMCID: PMC1279101  PMID: 7188967

Abstract

1. An electrophysiological study of ascending and descending connexions between the dorsal raphe region of the mesencephalic periaqueductal grey matter and the medial preoptic area has been performed in dioestrous female rats anaesthetized with urethane. 2. Extracellular action potentials recorded from 208 neurones in the medial preoptic area were analysed for a change in excitability following stimulation of the periaqueductal grey matter. 174 neurones were also tested for changes in excitability following stimulation of the mediobasal hypothalamus. 3. Stimulation of the periaqueductal grey matter at 1 Hz was rarely effective, but short trains of pulses (three at 100 Hz) usually caused an initial inhibition (62.5% of 208) of both projection identified and adjacent neurones of the medial preoptic area, at latencies of 5--90 msec (mean 34.1 +/- 1.4 msec). Inhibition following stimulation of the mediobasal hypothalamus occurred less frequently (34%) and at shorter latency (mean 12.0 +/- 1.8 msec; n = 48). 4. Less frequently (10.6%) periaqueductal grey matter stimulation caused an initial excitation of preoptic neurones at latencies of 15--180 msec, (mean 35.3 +/- 7.2). Initial excitation following mediobasal hypothalamus stimulation was stronger, occurred more frequently (29%) and at shorter latencies (range 3--60 msec, mean 13.1 +/- 1.5). Following such initial excitation, inhibition of spontaneous or ionophoretically evoked activity occurred more frequently following mediobasal hypothalamic stimulation, than after periaqueductal grey matter stimulation. 5. Twenty-four neurones displayed antidromic invasion following periaqueductal grey matter stimulation. Latencies for invasion ranged from 13 to 50 msec (mean 25.5 +/- 2.0 msec) and are suggestive of an unmyelinated projection. Occasionally an abrupt decrease in latency followed an increase in stimulus intensity. Antidromic invasion from mediobasal hypothalamus was characterized by a shorter latency (mean 12.5 +/- 0.7 msec; n = 43). A period of reduced excitability lasting 40--100 msec followed antidromic invasion from either site. 6. Antidromic responses to paired mediobasal hypothalamic or periaqueductal grey matter stimuli at 5 msec intervals revealed an increased latency of invasion of the second response, due to the partial refractory period of the neurone. Five cells showed a decreased latency of invasion at stimulus separations of 10--150 msec, interpreted as evidence of a supranormal period. Changes in conduction velocity during the supranormal period may give rise to a variable latency of invasion of spontaneously active cells. 7. These results provide evidence for direct, reciprocal connexions between the midbrain central grey and the medial preoptic area. These circuits may play a role in controlling neuroendocrine and behavioural aspects of reproductive functions.

Full text

PDF
53

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aghajanian G. K., Wang R. Y. Habenular and other midbrain raphe afferents demonstrated by a modified retrograde tracing technique. Brain Res. 1977 Feb 18;122(2):229–242. doi: 10.1016/0006-8993(77)90291-8. [DOI] [PubMed] [Google Scholar]
  2. Arendash G. W., Gallo R. V. Serotonin involvement in the inhibition of episodic luteinizing hormone release during electrical stimulation of the midbrain dorsal raphe nucleus in ovariectomized rats. Endocrinology. 1978 Apr;102(4):1199–1206. doi: 10.1210/endo-102-4-1199. [DOI] [PubMed] [Google Scholar]
  3. Azmitia E. C., Segal M. An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat. J Comp Neurol. 1978 Jun 1;179(3):641–667. doi: 10.1002/cne.901790311. [DOI] [PubMed] [Google Scholar]
  4. Barry J., Dubois M. P., Carette B. Immunofluorescence study of the preoptico-infundibular LRF neurosecretory pathway in the normal, gastrated or testosterone-treated male guinea pig. Endocrinology. 1974 Nov;95(5):1416–1423. doi: 10.1210/endo-95-5-1416. [DOI] [PubMed] [Google Scholar]
  5. Barry J., Dubois M. P., Poulain P. LRF producing cells of the mammalian hypothalamus. A fluorescent antibody study. Z Zellforsch Mikrosk Anat. 1973 Dec 31;146(3):351–366. doi: 10.1007/BF02346227. [DOI] [PubMed] [Google Scholar]
  6. COWAN W. M., RAISMAN G., POWELL T. P. THE CONNEXIONS OF THE AMYGDALA. J Neurol Neurosurg Psychiatry. 1965 Apr;28:137–151. doi: 10.1136/jnnp.28.2.137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Carrer H. F., Taleisnik S. Effect of mesencephalic stimulation on the release of gonadotrophins. J Endocrinol. 1970 Dec;48(4):527–539. doi: 10.1677/joe.0.0480527. [DOI] [PubMed] [Google Scholar]
  8. Conrad L. C., Leonard C. M., Pfaff D. W. Connections of the median and dorsal raphe nuclei in the rat: an autoradiographic and degeneration study. J Comp Neurol. 1974 Jul;156(2):179–205. doi: 10.1002/cne.901560205. [DOI] [PubMed] [Google Scholar]
  9. Conrad L. C., Pfaff D. W. Axonal projections of medial preoptic and anterior hypothalamic neurons. Science. 1975 Dec 12;190(4219):1112–1114. doi: 10.1126/science.1188390. [DOI] [PubMed] [Google Scholar]
  10. Conrad L. C., Pfaff D. W. Efferents from medial basal forebrain and hypothalamus in the rat. I. An autoradiographic study of the medial preoptic area. J Comp Neurol. 1976 Sep 15;169(2):185–219. doi: 10.1002/cne.901690205. [DOI] [PubMed] [Google Scholar]
  11. Cramer O. M., Barraclough C. A. Effects of preoptic electrical stimulation on pituitary LH release following interruption of components of the preoptico-tuberal pathway in rats. Endocrinology. 1973 Aug;93(2):369–376. doi: 10.1210/endo-93-2-369. [DOI] [PubMed] [Google Scholar]
  12. Dray A., Davies J., Oakley N. R., Tongroach P., Vellucci S. The dorsal and medial raphe projections to the substantia nigra in the rat: electrophysiological, biochemical and behavioural observations. Brain Res. 1978 Aug 11;151(3):431–442. doi: 10.1016/0006-8993(78)91077-6. [DOI] [PubMed] [Google Scholar]
  13. Dyer R. G. An electrophysiological dissection of the hypothalamic regions which regulate the pre-ovulatory secretion of luteinizing hormone in the rat. J Physiol. 1973 Oct;234(2):421–442. doi: 10.1113/jphysiol.1973.sp010352. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dyer R. G., Ellendorff F., MacLeod N. K. Non-random distribution of cell types in the preoptic and anterior hypothalamic areas. J Physiol. 1976 Oct;261(2):495–504. doi: 10.1113/jphysiol.1976.sp011570. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Dyer R. G., MacLeod N. K., Ellendorff F. Electrophysiological evidence for sexual dimorphism and synaptic convergence in the preoptic and anterior hypothalamic areas of the rat. Proc R Soc Lond B Biol Sci. 1976 Jun 30;193(1113):421–440. doi: 10.1098/rspb.1976.0055. [DOI] [PubMed] [Google Scholar]
  16. Ellendorff F., MacLeod N. K., Dyer R. G. Bipolar neurones in the rostral hypothalamus. Brain Res. 1976 Jan 23;101(3):549–553. doi: 10.1016/0006-8993(76)90477-7. [DOI] [PubMed] [Google Scholar]
  17. Fenske M., Ellendorff F., Wuttke W. Response of medial preoptic neurons to electrical stimulation of the mediobasal hypothalamus, amygdala and mesencephalon in normal, serotonin or catecholamine deprived female rats. Exp Brain Res. 1975 May 22;22(5):495–507. doi: 10.1007/BF00237350. [DOI] [PubMed] [Google Scholar]
  18. Field P. M. A quantitative ultrastructural analysis of the distribution of amygdaloid dibres in the preoptic area and the entromedial hypothalamic nucleus. Exp Brain Res. 1972 Apr 27;14(5):527–538. doi: 10.1007/BF00236594. [DOI] [PubMed] [Google Scholar]
  19. Fitzsimons J. T. Thirst. Physiol Rev. 1972 Apr;52(2):468–561. doi: 10.1152/physrev.1972.52.2.468. [DOI] [PubMed] [Google Scholar]
  20. Gardner C. R., Phillips S. W. Neuronal circuitry in the basal septum and preoptic area of the rat. Brain Res. 1977 Sep 9;133(1):95–106. doi: 10.1016/0006-8993(77)90051-8. [DOI] [PubMed] [Google Scholar]
  21. HARDY J. D., HELLON R. F., SUTHERLAND K. TEMPERATURE-SENSITIVE NEURONES IN THE DOG'S HYPOTHALAMUS. J Physiol. 1964 Dec;175:242–253. doi: 10.1113/jphysiol.1964.sp007515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Horrobin D. F. The lateral cervical nucleus of the cat; an electrophysiological study. Q J Exp Physiol Cogn Med Sci. 1966 Oct;51(4):351–371. doi: 10.1113/expphysiol.1966.sp001869. [DOI] [PubMed] [Google Scholar]
  23. Knigge K. M., Joseph S. A., Hoffman G. E. Organization of LRF-and SRIF-neurons in the endocrine hypothalamus. Res Publ Assoc Res Nerv Ment Dis. 1978;56:49–67. [PubMed] [Google Scholar]
  24. Köves K., Halász B. Location of the neural structures triggering ovulation in the rat. Neuroendocrinology. 1970;6(3):180–193. doi: 10.1159/000121922. [DOI] [PubMed] [Google Scholar]
  25. MacLeod N. K., Mayer M. L. Projection of the dorsal raphe nucleus on to identified preoptic neurones [proceedings]. J Physiol. 1978 Aug;281:27P–28P. [PubMed] [Google Scholar]
  26. Merrill E. G., Wall P. D., Yaksh T. L. Properties of two unmyelinated fibre tracts of the central nervous system: lateral Lissauer tract, and parallel fibres of the cerebellum. J Physiol. 1978 Nov;284:127–145. doi: 10.1113/jphysiol.1978.sp012531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Millhouse O. E. A Golgi study of the desending medial forebrain bundle. Brain Res. 1969 Oct;15(2):341–363. doi: 10.1016/0006-8993(69)90161-9. [DOI] [PubMed] [Google Scholar]
  28. Millhouse O. E. The organization of the ventromedial hypothalamic nucleus. Brain Res. 1973 May 30;55(1):71–87. [PubMed] [Google Scholar]
  29. Moore R. Y., Halaris A. E., Jones B. E. Serotonin neurons of the midbrain raphe: ascending projections. J Comp Neurol. 1978 Aug 1;180(3):417–438. doi: 10.1002/cne.901800302. [DOI] [PubMed] [Google Scholar]
  30. Moss R. L., Dudley C. A., Kelly M. J. Hypothalamic polypeptide releasing hormones: modifiers of neuronal activity. Neuropharmacology. 1978 Feb;17(2):87–93. doi: 10.1016/0028-3908(78)90119-3. [DOI] [PubMed] [Google Scholar]
  31. Moss R. L., Kelly M. J., Dudley C. A. Chemosensitivity of hypophysiotropic neurons to the microelectrophoresis of biogenic amines. Brain Res. 1978 Jan 6;139(1):141–152. doi: 10.1016/0006-8993(78)90066-5. [DOI] [PubMed] [Google Scholar]
  32. Perkins M. N., Whitehead S. A. Responses and pharmacological properties of preoptic/anterior hypothalamic neurones following medial forebrain bundle stimulation. J Physiol. 1978 Jun;279:347–360. doi: 10.1113/jphysiol.1978.sp012348. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Pfaff D., Keiner M. Atlas of estradiol-concentrating cells in the central nervous system of the female rat. J Comp Neurol. 1973 Sep 15;151(2):121–158. doi: 10.1002/cne.901510204. [DOI] [PubMed] [Google Scholar]
  34. Renaud L. P. Influence of amygdala stimulation on the activity of identified tuberoinfundibular neurones in the rat hypothalamus. J Physiol. 1976 Aug;260(1):237–252. doi: 10.1113/jphysiol.1976.sp011513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Renaud L. P. Influence of medial preoptic-anterior hypothalamic area stimulation of the excitability of mediobasal hypothalamic neurones in the rat. J Physiol. 1977 Jan;264(2):541–564. doi: 10.1113/jphysiol.1977.sp011682. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Saavedra J. M., Palkovits M., Brownstein M. J., Axelrod J. Serotonin distribution in the nuclei of the rat hypothalamus and preoptic region. Brain Res. 1974 Aug 30;77(1):157–165. doi: 10.1016/0006-8993(74)90812-9. [DOI] [PubMed] [Google Scholar]
  37. Sakumoto T., Tohyama M., Satoh K., Kimoto Y., Kinugasa T., Tanizawa O., Kurachi K., Shimizu N. Afferent fiber connections from lower brain stem to hypothalamus studied by the horseradish peroxidase method with special reference to noradrenaline innervation. Exp Brain Res. 1978 Jan 18;31(1):81–94. doi: 10.1007/BF00235806. [DOI] [PubMed] [Google Scholar]
  38. Siverman A. J., Krey L. C. The luteinizing hormone-releasing hormone (LH-RH) neuronal networks of the guinea pig brain. I. Intra- and extra-hypothalamic projections. Brain Res. 1978 Nov 24;157(2):233–246. doi: 10.1016/0006-8993(78)90026-4. [DOI] [PubMed] [Google Scholar]
  39. Swadlow H. A., Waxman S. G. Observations on impulse conduction along central axons. Proc Natl Acad Sci U S A. 1975 Dec;72(12):5156–5159. doi: 10.1073/pnas.72.12.5156. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Swadlow H. A., Waxman S. G., Rosene D. L. Latency variability and the identification of antidromically activated neurons in mammalian brain. Exp Brain Res. 1978 Jul 14;32(3):439–443. doi: 10.1007/BF00238715. [DOI] [PubMed] [Google Scholar]
  41. Swanson L. W. An autoradiographic study of the efferent connections of the preoptic region in the rat. J Comp Neurol. 1976 May 15;167(2):227–256. doi: 10.1002/cne.901670207. [DOI] [PubMed] [Google Scholar]
  42. Swanson L. W., Kucharczyk J., Mogenson G. J. Autoradiographic evidence for pathways from the medial preoptic area to the midbrain involved in the drinking response to angiotensin II. J Comp Neurol. 1978 Apr 15;178(4):645–659. doi: 10.1002/cne.901780404. [DOI] [PubMed] [Google Scholar]
  43. Willoughby J. O., Martin J. B. Pulsatile growth hormone secretion: inhibitory role of medial preoptic area. Brain Res. 1978 Jun 9;148(1):240–244. doi: 10.1016/0006-8993(78)90397-9. [DOI] [PubMed] [Google Scholar]
  44. van de Kar L. D., Lorens S. A. Differential serotonergic innervation of individual hypothalamic nuclei and other forebrain regions by the dorsal and median midbrain raphe nuclei. Brain Res. 1979 Feb 16;162(1):45–54. doi: 10.1016/0006-8993(79)90754-6. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES