Input from central nucleus of the amygdala efferents to pericoerulear dendrites, some of which contain tyrosine hydroxylase immunoreactivity

Light microscopic anterograde tracing studies indicate that neurons in the central nucleus of the amygdala (CNA) project to a region of the dorsal pontine tegmentum ventral to the superior cerebellar peduncle which contains noradrenergic dendrites of the nucleus locus coeruleus (LC). However, it has not been established whether the efferent terminals from the CNA target catecholamine‐containing dendrites of the LC or dendrites of neurons from neighboring nuclei which may extend into this region. To examine this question, we combined immunoperoxidase labeling of the anterograde tracer biotinylated dextran amine (BDA) from the CNA with immunogold‐silver labeling of the catecholamine‐synthesizing enzyme tryrosine hydroxylase (TH) in the rostrolateral LC region of adult rats. By light microscopy, BDA‐labeled processes were dense in the dorsal pons within the parabrachial nuclei as well as in the pericoerulear region immediately ventral to the superior cerebellar peduncle. Higher magnification revealed that BDA‐labeled varicose fibers overlapped TH‐labeled processes in this pericoerulear region. By electron microscopy, anterogradely labeled axon terminals contained small, clear as well as some large dense core vesicles and were commonly apposed to astrocytic processes along some portion of their plasmalemma. BDA‐labeled terminals mainly formed symmetric type synaptic contacts characteristic of inhibitory transmitters. Of 250 BDA‐labeled axon terminals examined where TH immunoreactivity was present in the neuropil, 81% contacted unlabeled and 19% contacted TH‐labeled dendrites. Additionally, amygdala efferents were often apposed to unlabeled axon terminals forming asymmetric (excitatory type) synapses. These results demonstrate that amygdaloid efferents may directly alter the activity of catecholaminergic and non‐catecholaminergic neurons in this pericoerulear region of the rat brain. Furthermore, our study suggests that CNA efferents may indirectly affect the activity of pericoerulear neurons through modulation of excitatory afferents. Amygdaloid projections to noradrenergic neurons may help integrate behavioral and visceral responses to threatening stimuli by influencing the widespread noradrenergic projections from the LC. © 1996 Wiley‐Liss, Inc.

[1]  C. Aoki,et al.  Optimization of differential immunogold-silver and peroxidase labeling with maintenance of ultrastructure in brain sections before plastic embedding , 1990, Journal of Neuroscience Methods.

[2]  D E Redmond,et al.  Current concepts. II. New evidence for a locus coeruleus-norepinephrine connection with anxiety. , 1979, Life sciences.

[3]  G. Aston-Jones,et al.  Locus coeruleus neurons in monkey are selectively activated by attended cues in a vigilance task , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  M Ennis,et al.  Dendrites of locus coeruleus neurons extend preferentially into two pericoerulear zones , 1996, The Journal of comparative neurology.

[5]  M. Palkovits,et al.  Stress-Induced Norepinephrine Release in the Hypothalamic Paraventricular Nucleus and Pituitary-Adrenocortical and Sympathoadrenal Activity: In Vivo Microdialysis Studies , 1995, Frontiers in Neuroendocrinology.

[6]  D. Amaral,et al.  The distribution of GABAergic cells, fibers, and terminals in the monkey amygdaloid complex: an immunohistochemical and in situ hybridization study , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  D. Hopkins Amygdalotegmental projections in the rat, cat and rhesus monkey , 1975, Neuroscience Letters.

[8]  L. Swanson The locus coeruleus: A cytoarchitectonic, golgi and immunohistochemical study in the albino rat , 1976, Brain Research.

[9]  Larry W. Swanson,et al.  Brain Maps: Structure of the Rat Brain , 1992 .

[10]  Gray Eg Axo-somatic and axo-dendritic synapses of the cerebral cortex: An electron microscope study , 1959 .

[11]  Masatoshi Tanaka,et al.  Involvement of the Brain Noradrenaline System in Emotional Changes Caused by Stress in Rats a , 1990, Annals of the New York Academy of Sciences.

[12]  D. Woodward,et al.  Interaction of norepinephrine with cerebrocortical activity evoked by stimulation of somatosensory afferent pathways in the rat , 1980, Experimental Neurology.

[13]  M. Zigmond,et al.  Prior exposure to chronic stress results in enhanced synthesis and release of hippocampal norepinephrine in response to a novel stressor , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  D. Compston,et al.  Growth factor stimulation triggers apoptotic cell death in mature oligodendrocytes , 1996, Journal of neuroscience research.

[15]  O. Bosler,et al.  Adrenergic neurons in the nucleus tractus solitarius receive GABAergic synapses. Demonstration by dual immunocytochemistry in the rat , 1989, Neuroscience Letters.

[16]  P Siekevitz,et al.  Isolation and characterization of postsynaptic densities from various brain regions: enrichment of different types of postsynaptic densities , 1980, The Journal of cell biology.

[17]  V. Tennyson The Fine Structure of the Nervous System. , 1970 .

[18]  G. Aston-Jones,et al.  Activation of locus coeruleus neurons by nucleus paragigantocellularis or noxious sensory stimulation is mediated by intracoerulear excitatory amino acid neurotransmission , 1992, Brain Research.

[19]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[20]  E. V. Van Bockstaele,et al.  Corticotropin‐releasing factor‐containing axon terminals synapse onto catecholamine dendrites and may presynaptically modulate other afferents in the rostral pole of the nucleus locus coeruleus in the rat brain , 1996, The Journal of comparative neurology.

[21]  Joseph E. LeDoux,et al.  Cardiovascular responses elicited by stimulation of neurons in the central amygdaloid nucleus in awake but not anesthetized rats resemble conditioned emotional responses , 1987, Brain Research.

[22]  G. Stock,et al.  Cardiovascular changes during arousal elicited by stimulation of amygdala, hypothalamus and locus coeruleus. , 1981, Journal of the autonomic nervous system.

[23]  T. Gray,et al.  Peptide injections into the amygdala of conscious rats: effects on blood pressure, heart rate and plasma catecholamines , 1988, Regulatory Peptides.

[24]  F. Bloom,et al.  Nonrepinephrine-containing locus coeruleus neurons in behaving rats exhibit pronounced responses to non-noxious environmental stimuli , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  P. Branchereau,et al.  Morphologically heterogeneous met‐enkephalin terminals form synapses with tyrosine hydroxylase‐containing dendrites in the rat nucleus locus coeruleus , 1995, The Journal of comparative neurology.

[26]  R. Roth,et al.  Increased turnover of norepinephrine in the rat cerebral cortex during stress: role of the locus coeruleus. , 1973, Neuropharmacology.

[27]  Charles J. Wilson,et al.  Fine structure of rat locus coeruleus , 1980, The Journal of comparative neurology.

[28]  V. M. Pickel,et al.  GABAergic neurons in rat nuclei of solitary tracts receive inhibitory‐type synapses from amygdaloid efferents lacking detectable GABA‐immunoreactivity , 1996, Journal of neuroscience research.

[29]  Floyd E. Bloom,et al.  Anatomy and physiology of locus coeruleus neurons: functional implications , 1984 .

[30]  Joseph E LeDoux,et al.  Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  M. Davis,et al.  Lesions of the central nucleus of the amygdala, but not the paraventricular nucleus of the hypothalamus, block the excitatory effects of corticotropin-releasing factor on the acoustic startle reflex , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  P. Goldman-Rakic,et al.  Selective prefrontal cortical projections to the region of the locus coeruleus and raphe nuclei in the rhesus monkey , 1984, Brain Research.

[33]  M. Cassell,et al.  Glycine elicits release of acetylcholine from the nucleus tractus solitarii in rat , 1994, Brain Research.

[34]  Gary Aston-Jones,et al.  Responses of primate locus coeruleus neurons to simple and complex sensory stimuli , 1988, Brain Research Bulletin.

[35]  U. Ungerstedt Stereotaxic mapping of the monoamine pathways in the rat brain. , 1971, Acta physiologica Scandinavica. Supplementum.

[36]  E. Reynolds THE USE OF LEAD CITRATE AT HIGH pH AS AN ELECTRON-OPAQUE STAIN IN ELECTRON MICROSCOPY , 1963, The Journal of cell biology.

[37]  G Chouvet,et al.  Afferent regulation of locus coeruleus neurons: anatomy, physiology and pharmacology. , 1991, Progress in brain research.

[38]  S. Foote,et al.  Effects of locus coeruleus activation on electroencephalographic activity in neocortex and hippocampus , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  S. Chiu,et al.  Neurotransmitter‐mediated signaling between axons and glial cells , 1994, Glia.

[40]  F. Bloom,et al.  Nucleus locus ceruleus: new evidence of anatomical and physiological specificity. , 1983, Physiological reviews.

[41]  V. Pickel,et al.  Neuropeptide Y and dynorphin‐immunoreactive large dense‐core vesicles are strategically localized for presynaptic modulation in the hippocampal formation and substantia nigra , 1995, Synapse.

[42]  T. Gray,et al.  Organization of amygdaloid projections to brainstem dopaminergic, noradrenergic, and adrenergic cell groups in the rat , 1992, Brain Research Bulletin.

[43]  R. Valentino,et al.  Pharmacology of locus coeruleus spontaneous and sensory-evoked activity. , 1991, Progress in brain research.

[44]  M. Page,et al.  Locus coeruleus activation by physiological challenges , 1994, Brain Research Bulletin.

[45]  R. Duman,et al.  Chronic antidepressant administration decreases the expression of tyrosine hydroxylase in the rat locus coeruleus. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[46]  S. Sesack,et al.  Dynorphin‐immunoreactive terminals in the rat nucleus accumbens: Cellular sites for modulation of target neurons and interactions with catecholamine afferents , 1994, The Journal of comparative neurology.

[47]  V. Pickel,et al.  Amygdala efferents form inhibitory‐type synapses with a subpopulation of catecholaminergic neurons in the rat nucleus tractus solitarius , 1995, The Journal of comparative neurology.

[48]  A. Kincaid,et al.  A species-specific population of tyrosine hydroxylase-immunoreactive neurons in the medial amygdaloid nucleus of the Syrian hamster , 1992, Brain Research.

[49]  D. Reis,et al.  Brain Catecholamines: Relation to Defense Reaction Evoked by Acute Brainstem Transection in Cat , 1967, Science.

[50]  P. Zhu,et al.  Exocytosis from large dense cored vesicles outside the active synaptic zones of terminals within the trigeminal subnucleus caudalis: A possible mechanism for neuropeptide release , 1986, Neuroscience.

[51]  S. Foote,et al.  Corticotropin-releasing factor in the locus coeruleus mediates EEG activation associated with hypotensive stress , 1993, Neuroscience Letters.

[52]  P. Hancock,et al.  A Dynamic Model of Stress and Sustained Attention , 1989, Human factors.

[53]  L. Swanson,et al.  The organization of projections from the central nucleus of the amygdala to brainstem sites involved in central autonomic regulation: A combined retrograde transport-immunohistochemical study , 1984, Brain Research.