The midbrain periaqueductal gray in the rat. II. A Golgi analysis
Alvin J. Beitz
Department of Veterinary Biology, University of Minnesota, St. Paul, Minnesota 55108
Search for more papers by this authorR. David Shepard
Department of Veterinary Biology, University of Minnesota, St. Paul, Minnesota 55108
Search for more papers by this authorAlvin J. Beitz
Department of Veterinary Biology, University of Minnesota, St. Paul, Minnesota 55108
Search for more papers by this authorR. David Shepard
Department of Veterinary Biology, University of Minnesota, St. Paul, Minnesota 55108
Search for more papers by this authorAbstract
This study consists of a detailed analysis of neurons in the midbrain periaqueductal gray of the rat utilizing four variants of the Golgi technique. Neurons were classified into three major categories based on soma shape, number of primary dendrites, number of dendritic bifurcations, interspinous distance, axonal origin, and axon trajectory. Neurons in each category were further subdivided into large and small varieties based predominantly on soma size and cendritic patterns. Both quantitative and qualitative data concerning each neuronal type is provided as well as data relating to its relative distribution among the four periaqueductal gray subdivisions. The small bipolar neuron, characterized by its small size and spindle-shaped soma, was the most prominent cell type observed, composing 37% of the impregnated neurons in our material. This cell type was most numerous in the medial subdivision and least prominent in the dorsolateral subdivision. The small triangular neuron composed 23% of the neuronal population and was relatively evenly distributed through the periaqueductal gray. The remaining four cell types include the large and small multipolar neurons, the large fusiform neurons, and the large triangular neurons. Axons originated from either the perikaryon or a proximal dendrite, with a dendritic origin being most common for large and small triangular neurons and large fusiform neurons. The trajectory of axons in single thick coronal sections originating from periaqueductal gray neurons is typically away from the mesencephalic aqueduct. The exact trajectory is dependent on the location of the neuron. Axons arising from cells in the dorsal subdivision usually project in a dorsal or dorsolateral direction while axons of ventrolateral neurons may project dorsally, laterally, or ventrally. In sum, these data indicate a complex level of internal organization of the periaqueductal gray. The results are discussed in terms of previous immunohistochemical studies of neurons in this region.
Literature Cited
- Arendash, G. W., and R. A. Gorski (1983) Suppression of lordotic responsiveness in the female rat during mesencephalic electrical stimulation. Pharmacol. Biochem. Behav. 19: 351–357.
-
Atrens, D. M.,
D. M., Cobin, and
G. Paxinos
(1977)
Reward-aversion analysis of rat mesencephalon.
Neurosci. Lett.
6:
197–201.
10.1016/0304-3940(77)90018-0 Google Scholar
- Bandler, R. (1982) Induction of ‘rage’ following microinjections of glutamate into midbrain but not hypothalamus of cats. Neurosci. Lett. 30: 183–188.
- Basbaum, A. I., and H. L. Fields (1984) Endogenous pain control systems: Brain stem spinal pathways and endorphin circuitry. Ann. Rev. Neurosci. 7: 309–338.
- Beitz, A. J. (1982a) The organization of afferent projections to the midbrain periaqueductal gray of the rat. Neuroscience 7: 133–159.
- Beitz, A. J. (1982b) The nuclei of origin of brain stem enkephalin and substance-P projections to the rodent nucleus raphe magnus. Neuroscience 7: 2753–2768.
- Beitz, A. J. (1985) The midbrain periaqueductal gray in the rat. I. Nuclear volume, cell number, density and orientation and regional subdivisions. J. Comp. Neurol 237: 445–459.
- Beitz, A. J., and V. Chan-Palay (1979) A Golgi analysis of neuronal organization in the medial cerebellar nucleus of the rat. Neuroscience 4: 47–63.
- Beitz, A. J., M. A., Mullett, and L. L. Weiner (1983a) The periaqueductal gray projections to the rat spinal trigeminal, raphe magnus, gigantocellular pars alpha and paragigantocellular nuclei arise from separate neurons. Brain Res. 258: 307–314.
- Beitz, A. J., R. D., Shepard, and W. E. Wells (1983b) The periaqueductal gray raphe magnus projection contains somatostatin, neurotensin and serotonin but not cholecystokinin. Brain Res. 267: 132–137.
- Braitenburg, V., V., Guglielmotti, and E. Sade (1967) Correlation of crystal growth with the staining of axons by the Golgi procedure. Stain Technol. 42: 277–283.
- Cannon, J. T., G. J., Prieto, A. Lee, and J. C. Liebeskind (1982) Evidence for opioid and non-opioid forms of stimulation-produced analgesia. Brain Res. 243: 315–321.
-
Cazala, P., and
A. M. Garrigues
(1983)
Effects of apomorphine clonidine or 5-methoxy-NN-dimethyl tryptamine on approach and escape components of lateral hypothalamus and mesencephalic central gray stimulation in two inbred strains of mice.
Pharmacol. Biochem. Behav.
18:
87–93.
10.1016/0091-3057(83)90256-3 Google Scholar
- Colonnier, M. (1964) The tangential organization of the visual cortex. J. Anat. 98: 327–344.
- Dennis, S. G., M., Choiniere, and R. Melzack (1980) Stimulation-produced analgesia in rats: Assessment by two pain tests and correlation with self-stimulation. Exp. Neurol. 68: 295–309.
- Fardin, V., J. L., Oliveras, and J. M. Besson (1964a) A reinvestigation of the analgesic effects induced by stimulation of the periaqueductal gray matter in the rat. I. The production of behavioral side effects together with analgesia. Brain Res. 306: 105–123.
- Fardin, V., J. L., Oliveras, and J. M. Besson (1984b) A reinvestigation of the analgesic effects induced by stimulation of the periaqueductal gray matter in the rat. II Differential characteristics of the analgesia induced by ventral and dorsal PAG stimulation. Brain Res. 306: 125–139.
- Gebhart, G. P., J., Sandkuhler, J. G. Thalhammer, and M. Zimmerman (1983) Inhibition of spinal nociceptive information by stimulation in midbrain of the cat is blocked by lidocaine microinjected in nucleus raphe magnus and medullary reticular formation. J. Neurophysiol. 50: 1446–1459.
- Gebhart, G. F., and J. R. Toleikis (1978) An evaluation of stimulation-produced analgesia in the cat. Exp. Neurol. 62: 570–579.
- Gerhart, K. D., R. P., Yezierski, T. K. Wilcox, and W. D. Willis (1984) Inhibition of primate spinothalamic tract neurons by stimulation in periaqueductal gray or adjacent midbrain reticular formation. J. Neurophysiol. 52: 450–466.
- Jurgens, V., and R. Pratt (1979) Role of the periaqueductal gray in vocal expression of emotion. Brain Res. 167: 367–387.
- Kayser, V., J. M., Benoist, and G. Guilbaud (1983) Low dose of morphine microinjected in the ventral periaqueductal gray matter of the rat depresses responses of nociceptive ventrobasal thalamic neurons. Neurosci. Lett. 37: 193–198.
- Laemle, L. K. (1979) Neuronal populations of the human periaqueductal gray, nucleus lateralis. J. Comp. Neurol. 186: 193–198.
- Larson, C. R., and M. K. Kistler (1984) Periaqueductal gray neuronal activity associated with laryngeal EMG and vocalization in the awake monkey. Neurosci. Lett. 46: 261–266.
- Lewis, V. A., and G. F. Gebhart (1977) Morphine-induced and stimulation-produced analgesias at coincident periaqueductal central gray loci: Evaluation of analgesic congruence, tolerance and cross-tolerance. Exp. Neurol. 57: 934–955.
- Liu, R. P. C. (1983) Laminar origins of spinal projection neurons to the periaqueductal gray of the rat. Brain Res. 264: 118–122.
- Liu, R. P. C., and B. L. Hamilton (1980) Neurons of the periaqueductal gray matter as revealed by Golgi study. J. Comp. Neurol. 189: 403–418.
- Magoun, H. W., D., Atlas, E. H. Ingersoll, and S. W. Ranson (1937) Associated facial, vocal and respiratory components of emotional expression: An experimental study. J. Neurol. Psychopathol. 17: 241–255.
- Mantyh, P. W. (1982a) The midbrain periaqueductal gray in the rat, cat and monkey: A Nissl, Weil and Golgi analysis. J. Comp. Neurol. 204: 349–363.
- Mantyh, P. W. (1982b) Forebrain projections to the periaqueductal gray in the monkey with observations in the cat and rat. J. Comp. Neurol. 206: 146–158.
- Mantyh, P. W. (1983a) Connections of midbrain periaqueductal gray in the monkey I. Ascending efferent projections. J. Neurophysiol. 49: 567–581.
- Mantyh, P. W. (1983b) Connections of midbrain periaqueductal gray in the monkey II. Descending efferent projections. J. Neurophysiol. 49: 582–594.
- Marchand, J. E., and N. Hagino (1983) Afferents to the periaqueductal gray in the rat. A horseradish peroxidase study. Neuroscience 9: 95–106.
- Martin, J. R. (1976) Motivated behavior elicited from hypothalamus, midbrain and pons of the guinea pig. (Cavia porcellus). J. Comp. Physiol. Psychol. 90: 1011–1034.
- Mayer, D. J., and J. C. Liebeskind (1974) Pain reduction by focal electrical stimulation of the brain: An anatomical and behavioral analysis. Brain Res. 68: 73–93.
- Morrell, J. I., L. M., Greenberger, and D. W. Pfaff (1981) Hypothalamic, other diencephalic and telencephalic neurons that project to the dorsal midbrain. J. Comp. Neurol. 201: 589–650.
- Mos, J., M. R. Kruk, A. M. Van der Poel, and W. Meelis (1982) Aggressive behavior induced by electrical stimulation in the midbrain central gray of male rats. Aggressive Behav. 8: 261–284.
- Mos, J., J. H. C. M. Lammers, A. M. Van der Poel, B. Bermond, W. Meelis, and M. R. Kruk (1983) Effects of midbrain central gray lesions on spontaneous and electrically induced aggression in the rat. Aggressive Behav, 9: 133–155.
- Moskowitz, A. S., and R. R. Goodman (1984) Light microscope autoradiographic localizations of μ and δ opioid binding sites in the mouse central nervous system. J. Neurosci. 4: 1331–1342.
- Moss, M. S., and A. I. Basbaum (1983) The peptidergic organization of the cat periaqueductal gray. II. The distribution of immunoreactive substance P and vasoactive intestinal polypeptide. J. Neurosci 3: 1437–1449.
- Moss, M. S., E. J., Glazer, and A. I. Basbaum (1983) The peptidergic organization of the cat periaqueductal gray. I. The distribution of immunoreactive enkephalin-containing neurons and terminals. J. Neurosci 3: 603–616.
-
Palay, S. L., and
V. Chan-Palay
(1974)
Cerebellar cortex: Cytology and Organization.
New York:
Springer,
pp. 322–336.
10.1007/978-3-642-65581-4_12 Google Scholar
- Prieto, G. J., Cannon J. T., and J. C. Liebeskind (1983) Raphe magnus lesions disrupt stimulation-produced analgesia from ventral but not dorsal areas in the rat. Brain Res. 261: 53–57.
- Ramon Moliner, E. (1957) A chlorate-formaldehyde modification of the Golgi method. Stain Technol. 32: 105–116.
- Ramón y Cajal, S. (1911) Histologie due Systèms Nerveux de l'homme et des Vertebrés, Vol. 2. Paris: Maloine, pp. 159–261.
- Reichling, D. B., S. F., Lakos, and A. I. Basbaum (1984) Intracellular electro-physiological and Golgi analysis of the midbrain periaqueductal gray (PAG) of the rat. Soc. Neurosci. Abstr. 10: 101.
- Ruda, M. T. (1976) Autoradiographic Study of the Efferent Projections of the Midbrain Central Gray in the Cat. Doctoral Thesis, University of Pennsylvania.
- Sakuma, Y., and D. W. Pfaff (1979) Mesencephalic Mechanisms for integration of female reproductive behavior in the rat. Am. J. Physiol. 237: R285–R290.
- Sakuma, Y. and D. W., Pfaff (1983) Modulation of the lordosis reflex of female rats by LHRH, its antiserum and analogs in the mesencephalic central gray. Neuroendocrinology 36: 218–224.
- Sirinathsinghi, D. J. S. (1984) Modulation of lordosis behavior of female rats by naloxone, β-endorphin and its antiserum in the mesencephalic central gray: Possible mediation via GnRH. Neuroendocrinology 39: 222–230.
- Skirboll, L., T., Hökfelt, G. Dockray, J. Rehfeld, M. Brownstein, and A. C. Cuello (1983) Evidence for periaqueductal gray cholecystokinin-substance P neurons projecting to spinal cord. J. Neurosci. 3: 1151–1157.
- Skultety, F. M. (1959) Relation of periaqueductal gray matter to stomach and bladder motility. Neurology 9: 190–197.
- Suka, N., P., Schlegel, T. Shimozawa, and J. Simmons (1973) Orientation sounds evoked from echolocating bats by electrical stimulation of the brain J. Acoust. Soc. Am. 54: 793–797.
- Thames, P. B., J. D., Trobe, and W. E. Ballinger (1984) Upgaze paralysis caused by lesion of the periaqueductal gray matter. Arch Neurol. 41: 437–440.
- Tredici, G., R., Bianchi, and M. Gioia (1983) Short intrinsic circuit in the periaqueductal gray matter of the cat. Neurosci. Lett. 39: 131–136.
- Van der Kooy, D., R. F. Mucha, M. O'Shaughnessy, and P. Bucenieks (1982) Reinforcing effects of brain microinjections of morphine revealed by conditioned place preference. Brain Res. 243: 107–117.
-
Valverde, P.
(1970)
The Golgi method. A tool for comparative structural analyses. In
W. J. H. Nauta and
S. O. E. Ebbesson (eds):
Contemporary Research Methods in Neuroanatomy.
New York:
Springer-Verlag,
pp. 12–31.
10.1007/978-3-642-85986-1_2 Google Scholar
- Waldbillig, R. J. (1975) Attack, eating, drinking and gnawing elicited by electrical stimulation of rat mesencephalon and pons. J. Comp. Physiol. Psychol. 39: 200–212.
- Willis, W. D., K. D., Gerhart, W. S. Willcockson, R. P. Yezierski, T. K. Wilcox, and C. L. Cargill (1984) Primate raphe and reticulospinal neurons: Effects of stimulation on periaqueductal gray or VPLc thalamic nucleus. J. Neurophysiol. 51: 467–480.
- Yaksh, T. L., J. L., Yeung, and T. A. Rudy (1976) Systematic examination in the rat of brain sites sensitive to direct application of morphine: Observations of differential effects within the PAG. Brain Res. 114: 83–94.
-
Young, E. G.,
L. R., Watkins, and
D. J. Mayer
(1984)
Comparison of the affects of ventral medullary lesions on systemic and microinjection morphine analgesia.
Brain Res.
290:
119–129.
10.1016/0006-8993(84)90741-8 Google Scholar