Anatomical identification of neurons in selected brain regions associated with maternal behavior deficits induced by knife cuts of the lateral hypothalamus in rats
Michael Numan
Department of Psychology, Boston College, Chestnut Hill, Massachusetts 02167
Search for more papers by this authorJoan I. Morrell
The Rockefeller University, New York, New York 10021
Search for more papers by this authorDonald W. Pfaff
The Rockefeller University, New York, New York 10021
Search for more papers by this authorMichael Numan
Department of Psychology, Boston College, Chestnut Hill, Massachusetts 02167
Search for more papers by this authorJoan I. Morrell
The Rockefeller University, New York, New York 10021
Search for more papers by this authorDonald W. Pfaff
The Rockefeller University, New York, New York 10021
Search for more papers by this authorAbstract
The present experiment identified neurons associated with maternal behavior deficits induced by damage to the lateral hypothalamus (LH) in rats. Fully maternal lactating rats received bilateral coronal knife cuts through either the dorsal or ventral LH at the level of the ventromedial nucleus. The blade of the wire knife used to make the cuts was coated with horseradish peroxidase (HRP). The maternal behavior of all females was studied for 4 days postoperatively and then the brains were processed for the localization of neurons retrogradely filled with HRP. The analysis focused on those brain regions thought to be important for maternal behavior.
The dorsal LH cuts severely disrupted maternal behavior while the ventral LH cuts did not. The ventral cuts labeled more medial preoptic area (MPOA) and septal-diagonal band neurons with HRP than did the dorsal cuts. The dorsal LH cuts labeled more neurons with HRP in the lateral preoptic area (LPOA), magnocellular preoptic area, bed nucleus of the stria terminalis, ventral tegmental area (VTA), substantia nigra, and central gray than did the ventral cuts.
Previous research has suggested that the lateral efferents of the MPOA interact with the VTA in the control of maternal behavior. The results of the present experiment suggest that MPOA axons which descend directly to the brainstem via the ventral LH are not essential for maternal behavior. Our results are consistent with the view that an MPOA-to-LPOA-to-VTA circuit may be important for maternal behavior.
Literature Cited
- Altar, A., K. A., Neve, S. E. Loughlin, J. F. Marshall, and J. H. Fallon (1983) The crossed mesostriatal projection: Neurochemistry and developmental response to lesion. Brain Res. 279: 1–8.
- Azmitia, E. G., and M. Segal (1978) An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat. J. Comp. Neurol. 179: 641–668.
- Barofsky, A., J., Taylor, Y. Tizabi, R. Kumar, and K. Jones-Quartey (1983) Specific neurotoxic lesions of median raphe serotonergic neurons disrupt maternal behavior in the lactating rat. Endocrinology 113: 1884–1893.
- Barone, F. C., M. J., Wayner, S. L. Scharoun, R. Guevara-Aguilar, and H. U. Aguilar-Baturoni (1981) Afferent connections to the lateral hypothalamus: A horseradish peroxidase study in the rat. Brain Res. Bull. 7: 75–88.
- Beckstead, R. M. (1979) An autoradiographic examination of cortico-cortical and subcortical projections of the mediodorsal projection (prefrontal) cortex in the rat. J. Comp. Neurol. 184: 43–62.
- Beckstead, R. M., V. B., Domesick, and W. J. H. Nauta (1979) Efferent connections of the substantia nigra and ventral tegmental area in the rat. Brain Res. 175: 191–217.
- Berk, M. L., and J. A. Finkelstein (1981) Afferent projections to the preoptic area and hypothalamic regions in the rat brain. Neuroscience 6: 1601–1624.
- Boulant, J. A. (1980) Hypothalamic control of thermoregulation: Neurophysiological basis. In P. J. Morgane and J. Panksepp (eds): Handbook of the Hypothalamus, Vol. 3, Part A, Behavioral Studies of the Hypothalamus. New York: Marcel Dekker, pp. 1–82.
- Conrad, L. C. A., and D. W. Pfaff (1976a) Efferents from medial basal forebrain and hypothalamus in the rat. I. An autoradiographic study of the medial preoptic area. J. Comp. Neurol. 169: 185–220.
- Conrad, L. C. A., and D. W. Pfaff (1976b) Autoradiographic tracing of nucleus accumbens efferents in the rat. Brain Res. 113: 589–596.
- De Groot, J. (1959) The rat forebrain in stereotaxic coordinates. Verh K. Ned. Arad Wet. Afd. Natuurkd. 52: 1–40.
- Epstein, A. N. (1982) The physiology of thirst. In D. W. Pfaff (ed): The Physiological Mechanisms of Motivation. New York: Springer-Verlag, pp. 164–214.
- Fahrbach, S. E., J. I., Morrell, and D. W. Pfaff (1984) Temporal pattern of HRP spread from an iontophoretic deposit site and description of a new HRP-gel implant method. J. Comp. Neurol. 225: 605–619.
- Fallon, J. H., and R. Y. Moore (1978) Catecholamine innervation of the basal forebrain. IV. Topography of the dopamine projection to the basal forebrain and neostriatum. J. Comp. Neurol. 180: 545–580.
- Fleischer, S., and B. M. Slotnick (1978) Disruption of maternal behavior in rats with lesions of the septal area. Physiol. Behav. 21: 189–200.
- Fleming, A. S., F., Vaccarino, and C. Luebke (1980) Amygdaloid inhibition of maternal behavior in the nulliparous female rat. Physiol. Behav. 25: 731–743.
- Jacobson, C. D., J., Terkel, R. A. Gorski, and C. H. Sawyer (1980) Effects of small medial preoptic area lesions on maternal behavior: Retrieving and nest building in the rat. Brain Res. 194: 471–478.
- Kita, H., and Y. Oomura (1982) An HRP study of the afferent connections of the rat lateral hypothalamic region. Brain Res. Bull. 8: 63–71.
- König, J. F. R., and R. A. Klippel (1963) The Rat Brain. Baltimore; Williams and Wilkins.
- Krettek, J. E., and J. L. Price (1978) Amygdaloid projections to subcortical structures within the banal forebrain and brainstem in the rat and cat. J. Comp. Neurol. 178: 225–254.
- Leonard, C. M. (1969) The prefrontal cortex of the rat. I. Cortical projection of the mediodorsal nucleus. II. Efferent connections. Brain Res. 12: 321–343.
-
Malsbury, C. and
D. W., Pfaff
(1974)
Neural and hormonal determinants of mating behavior in adult male rats: A review. In
L. Di Cara (ed):
Limbic and Autonomic Nervous Systems Research.
New York:
Plenum Press,
pp. 85–136.
10.1007/978-1-4613-4407-0_3 Google Scholar
- McNemar, Q. (1969) Psychological Statistics. New York: Wiley.
- Mesulam, M. M. (1978) Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: A non-carcinogenic blue reaction product with superior sensitivity for visualizing neuronal afferents and efferents. J. Histochem. Cytochem. 26: 106–117.
- Miceli, M. O., A. S., Fleming, and C. W. Malsbury (1983) Disruption of maternal behaviour in virgin and postparturient rats following sagittal plane knife cuts in the preoptic area–hypothalamus. Behav. Brain Res. 9: 337–360.
- Millhouse, O. E. (1969) A Golgi study of the descending medial forebrain bundle. Brain Res. 200: 47–57.
- Morrell, J. I., L. M., Greenberger, and D. W. Pfaff (1981) Comparison of horseradish peroxidase visualization methods: Quantitive results and further technical specifics. J. Histochem. Cytochem. 29: 903–916.
- Norgren, R. (1974) Gustatory afferents to ventral forebrain. Brain Res. 81: 285–295.
- Numan, M. (1974) Medial preoptic area and maternal behavior in the female rat. J. Comp. Physiol. Psychol. 87: 746–759.
-
Numan, M.
(1983)
Brain mechanisms of maternal behaviour in the rat. In
J. Balthazart,
E. Prove, and
R. Gilles (eds):
Hormones and Behaviour in Higher Vertebrates.
Berlin:
Springer-Verlag,
pp. 69–85.
10.1007/978-3-642-69216-1_6 Google Scholar
- Numan, M., and E. C. Callahan (1980) The connections of the medial preoptic region and maternal behavior in the rat. Physiol. Behav. 25: 653–665.
- Numan, M., and D. S. Nagle (1983) Preoptic area and substantia nigra interact in the control of maternal behavior in the rat. Behav. Neurosci. 97: 120–139.
- Numan, M., J. S., Rosenblatt, and B. R. Komisaruk (1977) Medial preoptic area and onset of maternal behavior in the rat. J. Comp. Physiol. Psychol. 91: 146–164.
- Numan, M., and H. G. Smith (1984) Maternal behavior in rats: Evidence for the involvement of preoptic projections to the ventral tegmental area. Behav. Neurosci. 98: 712–727.
-
Pfaff, D. W.
(1980)
Estrogens and Brain Function.
New York:
Springer-Verlag.
10.1007/978-1-4613-8084-9 Google Scholar
-
Pfaff, D. W.
(1982)
Neurobiological mechanisms of sexual motivation. In
D. W. Pfaff (ed):
The Physiological Mechanisms of Motivation.
New York:
Springer-Verlag,
pp. 287–317.
10.1007/978-1-4612-5692-2_10 Google Scholar
- Phillipson, O. T. (1979) Afferent projections to the ventral tegmental area of Tsai and interfascicular nucleus: A horseradish peroxidase study in the rat. J. Comp. Neurol. 187: 117–144.
- Raisman, G., and P. M. Field (1971) Anatomical considerations relevant to the interpretation of neuroendocrine experiments. In L. Martini and F. Ganong (eds): Frontiers in Neuroendocrinology. New York: Oxford University Press, pp. 3–44.
- Saper, C. B. (1982) Convergence of autonomic and limbic connections in the insular cortex of the rat. J. Comp. Neurol. 210: 163–173.
- Saper, C. B., and A. D. Loewy (1980) Efferent connections of the parabrachial nucleus in the rat. Brain Res. 197: 291–317.
- Sclafani, A., and S. P. Grossman (1969) Hyperphag a produced by knife cuts between the medial and lateral hypothalamus in the rat. Physiol. Beh. 4: 533–538.
- Scouten, C. W., C. W., Harley, and C. W. Malsbury (1982) Labeling knife cuts: A new method for revealing the functional anatomy of the CNS demonstrated on the noradrenergic dorsal bundle. Brain Res. Bull. 8: 229–232.
- Simon, H., M., LeMoal, and A. Calas (1979) Efferents and afferents of the ventral tegmental-A10 region studied after local injection of [3H] leucine and horseradish peroxidase. Brain Res. 178: 11–40.
- Steele, M. K., D., Rowland, and H. Moltz (1979) Initiation of maternal behavior in the rat: Possible involvement of limbic norepinephrine. Pharmac. Biochem. Behav. 11: 123–130.
- Stricker, E. M., and M. J. Zigmond (1976) Recovery of function after damage to central catecholamine containing neurons: A neurochemical model for the lateral hypothalamic syndrome. In J. M. Sprague and A. N. Epstein (eds): Progress in Psychobiology and Physiological Psychology, Vol. 6. New York: Academic Press, pp. 121–188.
- Swanson, L. W. (1976) An autoradiographic study of the efferent connections of the preoptic region in the rat. J. Comp. Neurol. 167: 227–256.
- Swanson, L. W. (1977) Immunohistochemical evidence for a neurophysin-containing autonomic pathway arising in the paraventricular nucleus of the hypothalamus. Brain Res. 128: 356–363.
- Swanson, L. W., and W. M. Cowan (1979) The connections of the septal region in the rat. J. Comp. Neurol. 186: 621–656.
- Terkel, J., R. S., Bridges, and C. H. Sawyer (1979) Effects of transecting lateral neural connections of the medial preoptic area on maternal behavior in the rat: Nest building, pup retrieval and prolactin secretion. Brain Res. 169: 369–380.
-
Ungerstedt, U.
(1971)
Stereotaxic mapping of the monoamine pathways in the rat brain.
Acta Physiol. Scand.
197:
[Suppl. 367]:
1–48.
10.1111/j.1365-201X.1971.tb10998.x Google Scholar
- Veening, J. G., L. W., Swanson, W. M. Cowan, R. Nieuwenhuys, and L. M. G. Geeraedts (1982) The medial forebrain bundle of the rat. II. An autoradiographic study of the topography of the major descending and ascending components. J. Comp. Neurol. 206: 82–108.
- Yamamoto, T., and Y. Shibata (1975) Direct Tiber connections between the frontal cortex and the hypothalamus in the rat: An electron microscopic study. Pharmacol. Biochem. Behav. 3: [Suppl. 1]: 15–22.