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Quiescence and hyporeactivity evoked by activation of cell bodies in the ventrolateral midbrain periaqueductal gray of the rat

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Abstract

Much evidence suggests that the midbrain periaqueductal gray region (PAG) plays a pivotal role in mediating an animal's responses to threatening, stressful, or painful stimuli. Active defensive reactions, hypertension, tachycardia and tachypnea are coordinated by a longitudinally oriented column of cells, found lateral to the midbrain aqueduct, in the caudal two-thirds of the PAG. In contrast, microinjections of excitatory amino acid (EAA) made in the ventrolateral region of the PAG in anesthetized or isolated animals evoke hypotension, bradycardia, and behavioral arrest. The aim of the present study was to examine further the effects of activation of neurons in the ventrolateral PAG. By injecting into this region low doses (40 pmol) of kainic acid (KA), a long-acting EAA, it was possible to observe a freely moving rat's behavior in a social situation (i.e., paired with a weight-matched, untreated partner). Such injected rats become quiescent, i.e., there was a cessation of all ongoing spontaneous activity. These rats were also hyporeactive: the investigative approaches of the partner failed to evoke orientation, startle reactions, or vocalization. Electroencephalographic measurements indicated that the effects of injections of KA in the ventrolateral PAG were not secondary to seizure activity. In addition to the quiescence and hyporeactivity reported here, and the hypotension and bradycardia reported previously, the ventrolateral PAG is a part of the brain from which analgesia has been readily evoked by electrical stimulation, or microinjections of either EAA or morphine. As a reaction to “deep” or “inescapable” pain, chronic injury, or defeat, animals often reduce their somatomotor activity, become more solitary, and are generally much less responsive to their environment. These data, and those from other recent studies, suggest that neurons in the ventrolateral PAG may play an important role in integrating such a passive behavioral response of which quiescence and hyporeactivity are the major components.

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References

  • Baghdoyan HA, Rodrigo-Angulo ML, McCarley RW, Hobson JA (1987) A neuroanatomical gradient in the pontine tegmentum for the cholinoceptive induction of desynchronized sleep signs. Brain Res 414:245–261

    Article  CAS  PubMed  Google Scholar 

  • Bandler R (1988) Brain mechanisms of aggression as revealed by electrical and chemical stimulation: suggestion of a central role for the midbrain periaqueductal grey region. In: Epstein A, Morrison A (eds) Progress in psychobiology and physiological psychology, vol 13. Academic Press, New York, pp 67–154

    Google Scholar 

  • Bandler R, Carrive P (1988) Integrated defence reaction elicited by excitatory amino acid injection in the midbrain periaqueductal grey region of the unrestrained cat. Brain Res 439:95–106

    Article  CAS  PubMed  Google Scholar 

  • Bandler R, Depaulis A (1988) Elicitation of intraspecific defence reactions in the rat from midbrain periaqueductal grey by microinjection of kainic acid, without neurotoxic effects. Neurosci Lett 88:291–296

    Google Scholar 

  • Bandler R, Depaulis A (1991) Midbrain periaqueductal gray control of defensive behavior in the cat and the rat. In: Depaulis A, Bandler R (eds) The midbrain periaqueductal gray matter: functional, anatomical and neurochemical organization. Plenum, New York, pp 175–198

    Google Scholar 

  • Bandler R, Carrive P, Zhang SP (1991a) Integration of somatic and autonomic reactions within the midbrain periaqueductal grey: viscerotopic, somatotopic and functional organization. Prog Brain Res 87:269–305

    Google Scholar 

  • Bandler R, Carrive P, Depaulis A (1991b) Emerging principles of organization of the midbrain periaqueductal gray matter. In: Depaulis A, Bandler R (eds) The midbrain periaqueductal gray matter: functional, anatomical and neurochemical organization. Plenum, New York, pp 1–8

    Google Scholar 

  • Blanchard RJ, Blanchard D C, Rodgers J, Weiss SM (1990) The characterization and modelling of antipredator defensive behavior. Neurosci Biobehav Rev 14:463–472

    Google Scholar 

  • Bolles RC, Fanselow MS (1980) A perceptual-defensive-recuperative model of fear and pain. Behav Brain Sci 3:291–301

    Google Scholar 

  • Carrive P (1991) Functional organization of PAG neurons controlling regional vascular beds. In: Depaulis A, Bandler R (eds) The midbrain periaqueductal gray matter: functional, anatomical and neurochemical organization. Plenum, New York, pp 67–100

    Google Scholar 

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

    Google Scholar 

  • Carrive P, Bandler R (1991b) Redistribution of blood flow in extracranial and hindlimb vascular beds evoked by excitation of neurons in the midbrain periaqueductal grey of the decerebrate cat. Exp Brain Res 84:599–606

    Google Scholar 

  • Carrive P, Dampney RAL, Bandler R (1987) Excitation of neurones in a restricted region of the midbrain periaqueductal grey elicits both behavioural and cardiovascular components of the defence reaction in the unanaesthetised decerebrate cat. Neurosci Lett 81:273–278

    Google Scholar 

  • Carrive P, Bandler R, Dampney, RAL (1989) Somatic and autonomic integration in the midbrain: a distinctive pattern evoked by excitation of neurones in the subtentorial portion of the midbrain periaqueductal grey region. Brain Res 483:251–258

    Google Scholar 

  • Depaulis A (1983) A microcomputer method for behavioural data acquisition and subsequent analysis. Pharmacol Biochem Behav 19:729–732

    Google Scholar 

  • Depaulis A (1992) Neuronal organization of intraspecific defensive behaviour in the periaqueductal gray matter of the rat. Neurosci Lett [Suppl] 42:S52

    Google Scholar 

  • Depaulis A, Bandler R, Vergnes M (1989) Characterization of pretentorial periaqueductal gray neurons mediating intraspecific defensive behaviors in the rat by microinjections of kainic acid. Brain Res 486:121–132

    Google Scholar 

  • Depaulis A, Keay KA, Bandler R (1992) Longitudinal neuronal organization of defensive reactions in the midbrain periaqueductal gray region of the rat. Exp Brain Res 90:307–318

    Google Scholar 

  • Fanselow M (1991) The midbrain periaqueductal gray as a coordinator of action in response to fear and anxiety. In: Depaulis A, Bandler R (eds) The midbrain periaqueductal gray matter: functional, anatomical and neurochemical organization, Plenum, New York, pp 151–174

    Google Scholar 

  • Fardin V, Oliveras JL, Besson JM (1984) 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 306:105–124

    Google Scholar 

  • Fidel de-la-Cruz JJ, Russek M (1987) Ontogeny of immobility reactions elicited by clamping, bandaging, and maternal transports in rats. Exp Neurol 97:315–326

    Google Scholar 

  • Fisher RS (1989) Animal models of the epilepsies. Brain Res Rev 14:245–278

    Google Scholar 

  • Fleischmann A, Urca G (1988) Different endogenous analgesia systems are activated by noxious stimulation of different body regions. Brain Res 455:49–57

    Google Scholar 

  • Fleischmann A, Urca G (1993) Tail-pinch induced analgesia and immobility: altered responses to noxious tail-pinch by prior pinch of the neck. Brain Res 601:28–33

    Google Scholar 

  • Fontani G, Vegni V (1990) Hippocampal electrical activity during social interactions in rabbits living in a seminatural environment. Physiol Behav 47:175–183

    Google Scholar 

  • Fontani G, Grazzi G, Lombardi G, Carli G (1982) Hippocampal rhythmic slow activity (RSA) during animal hypnosis in the rabbit. Behav Brain Res 6:15–24

    Google Scholar 

  • Grant EC, Mackintosh JH (1963) A comparison of the social postures of some common laboratory rodents. Behaviour 21:246–259

    Google Scholar 

  • Jensen TS, Yaksh TL (1992) Brainstem excitatory amino acid receptors in nociception: microinjection mapping and pharmacological characterization of glutamate-sensitive sites in the brainstem associated with algogenic behavior. Neurosci 46:535–547

    Google Scholar 

  • Katayama Y, DeWitt DS, Becker DP, Hayes RL (1984) Behavioral evidence for a cholinoceptive pontine inhibitory area: descending control of spinal motor output and sensory input. Brain Res 296:241–262

    Google Scholar 

  • Keay KA, Bandler R (1993) Deep and superficial noxious stimulation increases Fos-like immunoreactivity in different regions of the midbrain periaqueductal gray. Neurosci Lett 154:23–26

    Google Scholar 

  • Keay KA, Depaulis A, Bandler R (1992) “Deep” and “superficial” nociceptive stimulation evoke different behaviors and increase Fos-like immunoreactivity in distinct regions of spinal cord and midbrain periaqueductal gray. Soc Neurosci Abstr 11:832

    Google Scholar 

  • Keay KA, Clement CI, Owler B, Depaulis A, Bandler R (1994) Convergence of deep somatic and visceral nociceptive information onto a discrete ventrolateral midbrain periaqueductal gray region. Neuroscience (in press)

  • Lai YY, Siegel JM (1990) Cardiovascular and muscle tone changes produced by microinjection of cholinergic and glutamatergic agonists in dorsolateral pons and medial medulla. Brain Res 514:27–36

    Google Scholar 

  • Lewis T (1942) Pain. Macmillan, New York

    Google Scholar 

  • Lipski J, Bellingham MC, West MJ, Pilowsky P (1988) Limitations of the technique of pressure microinjection of excitatory amino acids for evoking responses from localized regions of the CNS. J Neurosci Methods 26:169–179

    Google Scholar 

  • Lovick TA (1991) Interactions between descending pathways from the dorsal and ventrolateral periaqueductal gray mater in the rat. In: Depaulis A, Bandler R (eds) The midbrain periaqueductal gray matter: functional, anatomical and neurochemical organization. Plenum, New York, pp 101–120

    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

    Google Scholar 

  • Maggio R, Liminga U, Gale K (1990) Selective stimulation of kainate but not quisqualate or NMDA receptors in substantia nigra evokes limbic motor seizures. Brain Res 528:223–230

    Google Scholar 

  • Miczek KA, Thompson ML, Shuster L (1982) Opioid-like analgesia in defeated mice. Science 215:1520–1522

    Google Scholar 

  • Mittler MM, Diment WC (1974) Cataleptic-like behavior in cats after microinjection of carbachol in the pontine reticular formation. Brain Res 68:335–343

    Google Scholar 

  • Morrison AR (1988) Paradoxical sleep without atonia. Arch Ital Biol. 126:275–289

    Google Scholar 

  • Paxinos G, Watson C (1982) The rat brain in stereotaxic coordinates. Academic Press, Sydney

    Google Scholar 

  • Piret B, Depaulis A, Vergnes M (1991) Opposite effects of agonist and inverse agonist ligands of benzodiazepine receptor on selfdefensive and submissive postures in the rat. Psychopharmacology 103:56–61

    Google Scholar 

  • Portavella M, Depaulis A, Vergnes M (1993) 22–28kHz ultrasonic vocalizations associated with defensive reactions in male rats do not result from fear or aversion. Psychopharmacology 111:190–194

    Google Scholar 

  • Quattrochi JJ, Namelak AN, Madison RD, Macklis JD, Hobson JA (1989) Mapping neuronal inputs to REM sleep induction sites with carbachol-fluorescent microspheres. Science 245:984–986

    Google Scholar 

  • Robinson TE (1980) Hippocampal rhythmic slow activity (RSA; theta): a critical analysis of selected studies and discussion of possible species differences. Brain Res Rev 2:69–101

    Google Scholar 

  • Rodgers RJ, Hendrie CA, Waters AJ (1983) Naloxone partially antagonizes post-encounter analgesia and enhances defensive responding in male rats exposed to attack from lactating conspecifics. Physiol Behav 30:781–786

    Google Scholar 

  • Shipley MT, Ennis M, Rizvi TA, Behbehani MM (1991) Topographical specificity of forebrain inputs to the midbrain periaqueductal gray: evidence for discrete longitudinally organized input columns. In: Depaulis A, Bandler R (eds) The midbrain periaqueductal gray matter: functional, anatomical and neurochemical organization, Plenum, New York, pp 417–448

    Google Scholar 

  • Wall PD (1979) On the relation of injury to pain. Pain 6:253–264

    Google Scholar 

  • Yaksh TL, Yeung JC, Rudy TA (1976) Systematic examination in the rat of brain sites sensitive to the direct application of morphine: observation of differential effects within the periaqueductal gray. Brain Res 114:83–103

    Google Scholar 

  • Zhang SP, Bandler R, Carrive P (1990) Flight and immobility evoked by excitatory amino acid microinjection within distinct parts of the subtentorial midbrain periaqueductal grey of the cat. Brain Res 520:73–82

    Google Scholar 

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Authors and Affiliations

  1. Neurobiologie et Neuropharmacologie des épilepsies généralisées, U.398 INSERM, Centre de Neurochimie, 5, rue Biaise Pascal, 67084, Strasbourg Cedex, France

    Antoine Depaulis

  2. Department of Anatomy and Histology, The University of Sydney, 2006, NSW, Australia

    Kevin A. Keay & Richard Bandler

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  1. Antoine Depaulis
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  2. Kevin A. Keay
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  3. Richard Bandler
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Depaulis, A., Keay, K.A. & Bandler, R. Quiescence and hyporeactivity evoked by activation of cell bodies in the ventrolateral midbrain periaqueductal gray of the rat. Exp Brain Res 99, 75–83 (1994). https://doi.org/10.1007/BF00241413

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  • DOI: https://doi.org/10.1007/BF00241413

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