Afferent and efferent connections of the cholinoceptive medial pontine reticular formation (region of the ventral tegmental nucleus) in the cat

G. R. Leichnetz, S. M. Carlton, Y. Katayama, A. Gonzalo-Ruiz, G. Holstege, A. A F Desalles, R. L. Hayes

Research output: Contribution to journalArticle

27 Citations (Scopus)

Abstract

Following minor concussive brain injury when there is an otherwise general suppression of CNS activity, the ventral tegmental nucleus of Gudden (VTN) demonstrates increased functional activity (32). Electrical or pharmacological activation of a cholinoceptive region in this same general area of the medial pontine tegmentum contributes to certain components of reversible traumatic unconsciousness, including postural atonia (31, 32, 45). Therefore, in an effort to examine the neuroanatomical basis of the behavioral suppression associated with a reversible traumatic unconsciousness, the afferent and efferent connections of the VTN and putative cholinoceptive medial pontine reticular formation (cmPRF) were studied in the cat using the retrograde horseradish peroxidase (HRP), HRP/choline acetyltransferase (ChAT) double-labeling immunohistochemistry, and anterograde HRP and autoradiographic techniques. Based upon retrograde HRP labeling, the principal afferents to the VTN region of the cmPRF originated from the medial and lateral mammillary nuclei, and lateral habenular nucleus, and to a lesser extent from the interpeduncular nucleus, lateral hypothalamus, dorsal tegmental nucleus, superior central nucleus, and contralateral nucleus reticularis pontis caudalis. Other afferents, which were thought to have been labeled through spread of HRP into the medial longitudinal fasciculus (MLF), adjacent paramedian pontine reticular formation, or uptake by transected fibers descending to the inferior olive, included the nucleus of Darkschewitsch, interstitial nucleus of Cajal, zona incerta, prerubral fields of Forel, deep superior colliculus, nucleus of the posterior commissure, nucleus cuneiformis, ventral periaqueductal gray, vestibular complex, perihypoglossal complex, and deep cerebellar nuclei. In HRP/ChAT double labeling studies, only a very small number of cholinergic VTN afferent neurons were found in the medial parabrachial region of the dorsolateral pontine tegmentum, although the pedunculopontine and laterodorsal tegmental nuclei contained numerous single-labeled ChAT-positive cells. Anterograde HRP and autoradiographic findings demonstrated that the VTN gave rise almost exclusively to ascending projections, which largely followed the course of the mammillary peduncle (16, 21) and medial forebrain bundle, or the tegmentopeduncular tract (4). The majority of fibers ascended to terminate in the medial and lateral mammillary nuclei, interpeduncular complex (especially paramedian subnucleus), ventral tegmental area, lateral hypothalamus, and the medial septum in the basal forebrain. Labeling that joined the mammillothalamic tract to terminate in the anterior nuclear complex of the thalamus was thought to occur transneuronally. Some projections were also observed to nucleus reticularis pontis oralis and caudalis, superior central nucleus, and dorsal tegmental nucleus adjacent to the VTN. Only when the injections involved more extensive portions of the rostral mPRF were projections to the intralaminar complex and reticular nucleus of the thalamus observed. Only meager descending projections were observed to the nucleus reticularis pontis caudalis and nucleus reticularis gigantocellularis of the rostral medulla, and none were observed to the spinal cord. While no functional significance could be attributed to the predominantly ascending limbic connections of the VTN, the lack of descending spinal connections, and the failure of these studies to find a major cholinergic input to a region purported to be the cholinoceptive pontine inhibitory area (CPIA), are discussed in relation to the possible neuroanatomical bases of the complex functional roles of the medial pontine tegmentum in the etiology of behavioral consequences following traumatic brain injury. Taken together with previous reports, the study suggests that the spinal-projecting portion of the CPIA responsible for muscular atonia is located in the medial brainstem tegmentum caudal to the VTN.

Original languageEnglish (US)
Pages (from-to)665-688
Number of pages24
JournalBrain Research Bulletin
Volume22
Issue number4
DOIs
StatePublished - 1989

Fingerprint

Tegmentum Mesencephali
Cats
Horseradish Peroxidase
Choline O-Acetyltransferase
Lateral Hypothalamic Area
Raphe Nuclei
Unconsciousness
Thalamus
Cholinergic Agents
Pedunculopontine Tegmental Nucleus
Pontine Tegmentum
Medial Forebrain Bundle
Habenula
Afferent Neurons
Cerebellar Nuclei
Periaqueductal Gray
Ventral Tegmental Area
Superior Colliculi
Brain Injuries
Brain Stem

Keywords

  • Autoradiography
  • Cat
  • Choline acetyltransferase immunohistochemistry
  • Cholinoceptive pontine inhibitory area
  • Coma
  • Consciousness
  • Horseradish peroxidase
  • Limbic system
  • Mammillary nuclei
  • Pontine reticular formation
  • Ventral tegmental nucleus

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Leichnetz, G. R., Carlton, S. M., Katayama, Y., Gonzalo-Ruiz, A., Holstege, G., Desalles, A. A. F., & Hayes, R. L. (1989). Afferent and efferent connections of the cholinoceptive medial pontine reticular formation (region of the ventral tegmental nucleus) in the cat. Brain Research Bulletin, 22(4), 665-688. https://doi.org/10.1016/0361-9230(89)90087-7

Afferent and efferent connections of the cholinoceptive medial pontine reticular formation (region of the ventral tegmental nucleus) in the cat. / Leichnetz, G. R.; Carlton, S. M.; Katayama, Y.; Gonzalo-Ruiz, A.; Holstege, G.; Desalles, A. A F; Hayes, R. L.

In: Brain Research Bulletin, Vol. 22, No. 4, 1989, p. 665-688.

Research output: Contribution to journalArticle

Leichnetz, G. R. ; Carlton, S. M. ; Katayama, Y. ; Gonzalo-Ruiz, A. ; Holstege, G. ; Desalles, A. A F ; Hayes, R. L. / Afferent and efferent connections of the cholinoceptive medial pontine reticular formation (region of the ventral tegmental nucleus) in the cat. In: Brain Research Bulletin. 1989 ; Vol. 22, No. 4. pp. 665-688.
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abstract = "Following minor concussive brain injury when there is an otherwise general suppression of CNS activity, the ventral tegmental nucleus of Gudden (VTN) demonstrates increased functional activity (32). Electrical or pharmacological activation of a cholinoceptive region in this same general area of the medial pontine tegmentum contributes to certain components of reversible traumatic unconsciousness, including postural atonia (31, 32, 45). Therefore, in an effort to examine the neuroanatomical basis of the behavioral suppression associated with a reversible traumatic unconsciousness, the afferent and efferent connections of the VTN and putative cholinoceptive medial pontine reticular formation (cmPRF) were studied in the cat using the retrograde horseradish peroxidase (HRP), HRP/choline acetyltransferase (ChAT) double-labeling immunohistochemistry, and anterograde HRP and autoradiographic techniques. Based upon retrograde HRP labeling, the principal afferents to the VTN region of the cmPRF originated from the medial and lateral mammillary nuclei, and lateral habenular nucleus, and to a lesser extent from the interpeduncular nucleus, lateral hypothalamus, dorsal tegmental nucleus, superior central nucleus, and contralateral nucleus reticularis pontis caudalis. Other afferents, which were thought to have been labeled through spread of HRP into the medial longitudinal fasciculus (MLF), adjacent paramedian pontine reticular formation, or uptake by transected fibers descending to the inferior olive, included the nucleus of Darkschewitsch, interstitial nucleus of Cajal, zona incerta, prerubral fields of Forel, deep superior colliculus, nucleus of the posterior commissure, nucleus cuneiformis, ventral periaqueductal gray, vestibular complex, perihypoglossal complex, and deep cerebellar nuclei. In HRP/ChAT double labeling studies, only a very small number of cholinergic VTN afferent neurons were found in the medial parabrachial region of the dorsolateral pontine tegmentum, although the pedunculopontine and laterodorsal tegmental nuclei contained numerous single-labeled ChAT-positive cells. Anterograde HRP and autoradiographic findings demonstrated that the VTN gave rise almost exclusively to ascending projections, which largely followed the course of the mammillary peduncle (16, 21) and medial forebrain bundle, or the tegmentopeduncular tract (4). The majority of fibers ascended to terminate in the medial and lateral mammillary nuclei, interpeduncular complex (especially paramedian subnucleus), ventral tegmental area, lateral hypothalamus, and the medial septum in the basal forebrain. Labeling that joined the mammillothalamic tract to terminate in the anterior nuclear complex of the thalamus was thought to occur transneuronally. Some projections were also observed to nucleus reticularis pontis oralis and caudalis, superior central nucleus, and dorsal tegmental nucleus adjacent to the VTN. Only when the injections involved more extensive portions of the rostral mPRF were projections to the intralaminar complex and reticular nucleus of the thalamus observed. Only meager descending projections were observed to the nucleus reticularis pontis caudalis and nucleus reticularis gigantocellularis of the rostral medulla, and none were observed to the spinal cord. While no functional significance could be attributed to the predominantly ascending limbic connections of the VTN, the lack of descending spinal connections, and the failure of these studies to find a major cholinergic input to a region purported to be the cholinoceptive pontine inhibitory area (CPIA), are discussed in relation to the possible neuroanatomical bases of the complex functional roles of the medial pontine tegmentum in the etiology of behavioral consequences following traumatic brain injury. Taken together with previous reports, the study suggests that the spinal-projecting portion of the CPIA responsible for muscular atonia is located in the medial brainstem tegmentum caudal to the VTN.",
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T1 - Afferent and efferent connections of the cholinoceptive medial pontine reticular formation (region of the ventral tegmental nucleus) in the cat

AU - Leichnetz, G. R.

AU - Carlton, S. M.

AU - Katayama, Y.

AU - Gonzalo-Ruiz, A.

AU - Holstege, G.

AU - Desalles, A. A F

AU - Hayes, R. L.

PY - 1989

Y1 - 1989

N2 - Following minor concussive brain injury when there is an otherwise general suppression of CNS activity, the ventral tegmental nucleus of Gudden (VTN) demonstrates increased functional activity (32). Electrical or pharmacological activation of a cholinoceptive region in this same general area of the medial pontine tegmentum contributes to certain components of reversible traumatic unconsciousness, including postural atonia (31, 32, 45). Therefore, in an effort to examine the neuroanatomical basis of the behavioral suppression associated with a reversible traumatic unconsciousness, the afferent and efferent connections of the VTN and putative cholinoceptive medial pontine reticular formation (cmPRF) were studied in the cat using the retrograde horseradish peroxidase (HRP), HRP/choline acetyltransferase (ChAT) double-labeling immunohistochemistry, and anterograde HRP and autoradiographic techniques. Based upon retrograde HRP labeling, the principal afferents to the VTN region of the cmPRF originated from the medial and lateral mammillary nuclei, and lateral habenular nucleus, and to a lesser extent from the interpeduncular nucleus, lateral hypothalamus, dorsal tegmental nucleus, superior central nucleus, and contralateral nucleus reticularis pontis caudalis. Other afferents, which were thought to have been labeled through spread of HRP into the medial longitudinal fasciculus (MLF), adjacent paramedian pontine reticular formation, or uptake by transected fibers descending to the inferior olive, included the nucleus of Darkschewitsch, interstitial nucleus of Cajal, zona incerta, prerubral fields of Forel, deep superior colliculus, nucleus of the posterior commissure, nucleus cuneiformis, ventral periaqueductal gray, vestibular complex, perihypoglossal complex, and deep cerebellar nuclei. In HRP/ChAT double labeling studies, only a very small number of cholinergic VTN afferent neurons were found in the medial parabrachial region of the dorsolateral pontine tegmentum, although the pedunculopontine and laterodorsal tegmental nuclei contained numerous single-labeled ChAT-positive cells. Anterograde HRP and autoradiographic findings demonstrated that the VTN gave rise almost exclusively to ascending projections, which largely followed the course of the mammillary peduncle (16, 21) and medial forebrain bundle, or the tegmentopeduncular tract (4). The majority of fibers ascended to terminate in the medial and lateral mammillary nuclei, interpeduncular complex (especially paramedian subnucleus), ventral tegmental area, lateral hypothalamus, and the medial septum in the basal forebrain. Labeling that joined the mammillothalamic tract to terminate in the anterior nuclear complex of the thalamus was thought to occur transneuronally. Some projections were also observed to nucleus reticularis pontis oralis and caudalis, superior central nucleus, and dorsal tegmental nucleus adjacent to the VTN. Only when the injections involved more extensive portions of the rostral mPRF were projections to the intralaminar complex and reticular nucleus of the thalamus observed. Only meager descending projections were observed to the nucleus reticularis pontis caudalis and nucleus reticularis gigantocellularis of the rostral medulla, and none were observed to the spinal cord. While no functional significance could be attributed to the predominantly ascending limbic connections of the VTN, the lack of descending spinal connections, and the failure of these studies to find a major cholinergic input to a region purported to be the cholinoceptive pontine inhibitory area (CPIA), are discussed in relation to the possible neuroanatomical bases of the complex functional roles of the medial pontine tegmentum in the etiology of behavioral consequences following traumatic brain injury. Taken together with previous reports, the study suggests that the spinal-projecting portion of the CPIA responsible for muscular atonia is located in the medial brainstem tegmentum caudal to the VTN.

AB - Following minor concussive brain injury when there is an otherwise general suppression of CNS activity, the ventral tegmental nucleus of Gudden (VTN) demonstrates increased functional activity (32). Electrical or pharmacological activation of a cholinoceptive region in this same general area of the medial pontine tegmentum contributes to certain components of reversible traumatic unconsciousness, including postural atonia (31, 32, 45). Therefore, in an effort to examine the neuroanatomical basis of the behavioral suppression associated with a reversible traumatic unconsciousness, the afferent and efferent connections of the VTN and putative cholinoceptive medial pontine reticular formation (cmPRF) were studied in the cat using the retrograde horseradish peroxidase (HRP), HRP/choline acetyltransferase (ChAT) double-labeling immunohistochemistry, and anterograde HRP and autoradiographic techniques. Based upon retrograde HRP labeling, the principal afferents to the VTN region of the cmPRF originated from the medial and lateral mammillary nuclei, and lateral habenular nucleus, and to a lesser extent from the interpeduncular nucleus, lateral hypothalamus, dorsal tegmental nucleus, superior central nucleus, and contralateral nucleus reticularis pontis caudalis. Other afferents, which were thought to have been labeled through spread of HRP into the medial longitudinal fasciculus (MLF), adjacent paramedian pontine reticular formation, or uptake by transected fibers descending to the inferior olive, included the nucleus of Darkschewitsch, interstitial nucleus of Cajal, zona incerta, prerubral fields of Forel, deep superior colliculus, nucleus of the posterior commissure, nucleus cuneiformis, ventral periaqueductal gray, vestibular complex, perihypoglossal complex, and deep cerebellar nuclei. In HRP/ChAT double labeling studies, only a very small number of cholinergic VTN afferent neurons were found in the medial parabrachial region of the dorsolateral pontine tegmentum, although the pedunculopontine and laterodorsal tegmental nuclei contained numerous single-labeled ChAT-positive cells. Anterograde HRP and autoradiographic findings demonstrated that the VTN gave rise almost exclusively to ascending projections, which largely followed the course of the mammillary peduncle (16, 21) and medial forebrain bundle, or the tegmentopeduncular tract (4). The majority of fibers ascended to terminate in the medial and lateral mammillary nuclei, interpeduncular complex (especially paramedian subnucleus), ventral tegmental area, lateral hypothalamus, and the medial septum in the basal forebrain. Labeling that joined the mammillothalamic tract to terminate in the anterior nuclear complex of the thalamus was thought to occur transneuronally. Some projections were also observed to nucleus reticularis pontis oralis and caudalis, superior central nucleus, and dorsal tegmental nucleus adjacent to the VTN. Only when the injections involved more extensive portions of the rostral mPRF were projections to the intralaminar complex and reticular nucleus of the thalamus observed. Only meager descending projections were observed to the nucleus reticularis pontis caudalis and nucleus reticularis gigantocellularis of the rostral medulla, and none were observed to the spinal cord. While no functional significance could be attributed to the predominantly ascending limbic connections of the VTN, the lack of descending spinal connections, and the failure of these studies to find a major cholinergic input to a region purported to be the cholinoceptive pontine inhibitory area (CPIA), are discussed in relation to the possible neuroanatomical bases of the complex functional roles of the medial pontine tegmentum in the etiology of behavioral consequences following traumatic brain injury. Taken together with previous reports, the study suggests that the spinal-projecting portion of the CPIA responsible for muscular atonia is located in the medial brainstem tegmentum caudal to the VTN.

KW - Autoradiography

KW - Cat

KW - Choline acetyltransferase immunohistochemistry

KW - Cholinoceptive pontine inhibitory area

KW - Coma

KW - Consciousness

KW - Horseradish peroxidase

KW - Limbic system

KW - Mammillary nuclei

KW - Pontine reticular formation

KW - Ventral tegmental nucleus

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